Please wait a minute...
Frontiers of Environmental Science & Engineering

ISSN 2095-2201

ISSN 2095-221X(Online)

CN 10-1013/X

Postal Subscription Code 80-973

2018 Impact Factor: 3.883

Front. Environ. Sci. Eng.    2015, Vol. 9 Issue (2) : 259-268    https://doi.org/10.1007/s11783-014-0652-2
RESEARCH ARTICLE
Phytotoxicity in seven higher plant species exposed to di-n-butyl phthalate or bis (2-ethylhexyl) phthalate
Tingting MA1,2, Ying TENG1,2, Peter CHRISTIE3, Yongming LUO1,2,4()
1. Key Laboratory of Soil Environment and Pollution Remediation of Chinese Academy of Sciences, Institute of Soil Science, Nanjing 210008, China
2. Graduate University of Chinese Academy of Sciences, Beijing 100049, China
3. Agri-Environment Branch, Agri-Food and Biosciences Institute, Newforge Lane, Belfast BT9 5PX, United Kingdom
4. Yantai Institute of Costal Zone Research, Chinese Academy of Sciences, Yantai 264003, China
 Download: PDF(240 KB)   HTML
 Export: BibTeX | EndNote | Reference Manager | ProCite | RefWorks
Abstract

We investigated phytotoxicity in seven plant species exposed to a range of concentrations (0– 500 mg·kg−1 soil) of di-n-butyl phthalate (DnBP) or bis (2-ethylhexyl) phthalate (DEHP), two representative phthalate esters (PAEs) nominated by USEPA as priority pollutants and known environmental estrogens. We studied seed germination, root elongation, seedling growth, biomass (fresh weight, FW) and malondialdehyde (MDA) content of shoots and roots of wheat (Triticum aestivum L.), alfalfa (Medicago sativa L.), perennial ryegrass (Lolium perenne), radish (Raphanus sativus L.), cucumber (Cucumis sativus L.), oat (Avena sativa) and onion (Allium cepa L.), together with monitoring of plant pigment content (chlorophyll a, b and carotinoids) in alfalfa, radish and onion shoots. Root elongation, seedling growth and biomass of the test species were generally inhibited by DnBP but not by DEHP, indicating a lower level of phytotoxicity of DEHP than of DnBP. MDA contents of four species were promoted by PAE exposure, but not in alfalfa, ryegrass or onion shoots, indicating lower sensitivity of these three species to PAE pollutants. Plant pigment contents were clearly affected under the stress of both pollutants, implying the potential damage to the photosynthetic system of test plants, mainly by decreasing the content of chlorophyll a and b. Results of DnBP and DEHP phytotoxicity to the primary growth of test plants has provided information for the assessment of their environmental risk in the soil and also forms a basis for the further analysis of their toxic effects over the whole growth period of different plant species.

Keywords phytotoxicity      di-n-butyl phthalate      bis(2-ethylhexyl) phthalate      malondialdehyde      plant pigments (chlorophyll a      b and carotinoids)     
Corresponding Author(s): Yongming LUO   
Online First Date: 21 February 2014    Issue Date: 13 February 2015
 Cite this article:   
Tingting MA,Ying TENG,Peter CHRISTIE, et al. Phytotoxicity in seven higher plant species exposed to di-n-butyl phthalate or bis (2-ethylhexyl) phthalate[J]. Front. Environ. Sci. Eng., 2015, 9(2): 259-268.
 URL:  
https://academic.hep.com.cn/fese/EN/10.1007/s11783-014-0652-2
https://academic.hep.com.cn/fese/EN/Y2015/V9/I2/259
PAE concentration/(mg·kg−1) germination rate/%
wheat alfalfa ryegrass radish cucumber oat onion
DnBP 0 (CK) 95.5 90.5 96.5 98.0 92.5 95.0 95.5
5 95.0 89.5 96.0 97.5 90.5 93.0 95.0
20 95.0 90.0 96.0 97.0 90.0 94.5 94.0
100 94.5 90.0 95.5 98.0 91.0 94.0 95.0
500 94.0 90.0 97.0 97.0 90.0 94.0 94.0
DEHP 0 (CK) 95.5 90.5 96.5 98.0 92.0 95.0 95.5
5 94.5 90.5 96.0 96.0 90.0 95.0 95.0
20 95.0 90.0 96.0 97.0 90.0 93.5 95.5
100 94.0 89.0 97.0 96.5 91.5 94.0 94.0
500 93.5 90.0 96.0 96.0 91.0 95.5 94.5
Tab.1  Seed germination rates of the seven test plant species exposed to DnBP or DEHP a)
species pollutant root elongation/cm seedling growth/cm biomass (g)
0/CK 5 20 100 500 0/CK 5 20 100 500 0/CK 5 20 100 500
wheat DnBP 3.33±0.13 3.51±0.14* 3.55±0.10* 3.07±0.08* 2.63±0.08* 1.57±0.11 1.50±0.03 1.41±0.11 1.18±0.06 1.01±0.02 5.60±0.31 5.17±0.30 5.14±0.15* 4.98±0.74* 4.44±0.12*
DEHP 3.90±0.08 3.51±0.07* 3.56±0.13* 3.16±0.03* 3.19±0.07* 1.52±0.03 1.43±0.03* 1.49±0.07 1.49±0.05 1.46±0.03 5.21±0.04 4.87±0.07* 4.40±0.20* 4.94±0.11* 4.57±0.06*
alfalfa DnBP 1.97±0.09 1.66±0.04* 1.63±0.16* 1.53±0.06* 1.48±0.08* 1.55±0.08 1.33±0.06* 1.29±0.09* 1.19±0.04* 1.19±0.06* 0.94±0.02 0.84±0.01* 0.85±0.01* 0.85±0.06* 0.79±0.02*
DEHP 2.24±0.09 1.68±0.02* 1.62±0.08* 1.75±0.06* 1.74±0.07* 1.53±0.03 1.42±0.05* 1.47±0.05* 1.41±0.04* 1.38±0.01* 1.04±0.09 0.82±0.04* 0.95±0.01 0.84±0.04 0.89±0.07*
ryegrass DnBP 1.76±0.04 1.93±0.09* 1.81±0.04 1.56±0.02* 1.65±0.03* 0.97±0.02 1.05±0.02* 1.06±0.06* 1.06±0.01* 0.89±0.03* 0.76±0.01 0.66±0.04* 0.77±0.03 0.64±0.04* 0.64±0.03*
DEHP 1.78±0.01 1.81±0.06 1.62±0.03* 2.05±0.06* 2.13±0.05* 1.01±0.13 1.00±0.04 0.79±0.03* 1.46±0.03* 1.33±0.10* 0.80±0.02 0.76±0.03 0.69±0.03* 0.84±0.03 0.77±0.04
radish DnBP 3.44±0.33 3.25±0.10 3.39±0.11 3.35±0.16 2.89±0.11* 0.93±0.10 0.91±0.04 0.90±0.03 0.97±0.11 0.89±0.08 2.68±0.16 1.97±0.06* 2.22±0.09* 1.75±0.08* 2.21±0.11*
DEHP 2.58±0.02 3.26±0.03* 2.85±0.02* 2.88±0.03* 3.36±0.09* 1.04±0.11 1.31±0.04* 1.11±0.02 0.98±0.09 1.16±0.04 1.93±0.12 2.25±0.24* 2.35±0.19* 2.22±0.23* 2.19±0.05*
cucumber DnBP 1.99±0.06 1.68±0.18* 1.30±0.09* 1.91±0.05 1.63±0.09* 0.65±0.03 0.58±0.08 0.71±0.07 0.65±0.07 0.72±0.03 4.34±0.11 3.62±0.11 4.07±0.06 4.47±0.11 3.87±0.11
DEHP 1.57±0.13 1.28±0.11* 1.65±0.09 1.81±0.16* 1.84±0.21* 0.9±0.07 0.57±0.06* 0.74±0.03* 0.67±0.05* 0.55±0.05* 3.67±0.12 3.85±0.05* 3.79±0.03 4.05±0.07* 3.82±0.11*
oat DnBP 2.15±0.08 2.26±0.10 2.16±0.08 1.77±0.11* 1.60±0.09* 1.09±0.05 1.10±0.06 0.97±0.07* 0.93±0.05* 0.87±0.01* 2.65±0.12 2.85±0.05* 2.44±0.06* 2.51±0.05* 2.40±0.05*
DEHP 2.20±0.15 2.30±0.09 2.10±0.06 2.34±0.08 2.29±0.09 1.23±0.05 1.05±0.06* 1.06±0.05* 1.14±0.08 1.28±0.07 3.07±0.08 2.83±0.09* 2.51±0.09* 2.87±0.10* 3.03±0.09
common onion b) DnBP 1.35±0.05 1.17±0.07* 0.87±0.06* 0.86±0.04* 0.77±0.053* 2.55±0.05 2.11±0.07* 1.86±0.11* 1.59±0.03* 1.87±0.11* 1.08±0.09 0.80±0.05* 0.75±0.02* 0.60±0.08* 0.62±0.02*
DEHP 0.92±0.08 1.16±0.17* 0.98±0.17 1.16±0.04* 1.37±0.07* 1.64±0.19 1.99±0.13* 1.76±0.11 1.88±0.13* 2.21±0.19* 0.75±0.04 0.75±0.19 0.75±0.06 0.73±0.02 0.84±0.04
Tab.2  Seedling root elongation, growth and biomass (FW) of seven test plant species exposed to different PAE treatments a)
plant species test part MDA content/(nmol·g−1) under DnBP treatment MDA content/(nmol·g−1) under DEHP treatment
0/CK 5 20 100 500 0/CK 5 20 100 500
wheat shoot 0.58±0.03 0.61±0.02 0.59±0.01 0.64±0.02 0.60±0.02 0.58±0.03 0.56±0.02* 0.41±0.02* 0.47±0.02* 0.53±0.02*
root 0.65±0.02 0.97±0.03* 0.82±0.02* 0.72±0.02 0.78±0.02* 0.65±0.02 0.91±0.03* 0.87±0.02* 0.72±0.02* 0.71±0.02*
alfalfa shoot 6.74±0.33 7.53±0.31* 6.94±0.28* 5.99±0.32* 5.94±0.37* 6.74±0.33 7.53±0.22* 6.24±0.31* 4.94±0.38* 4.94±0.33*
root 5.73±0.27 7.91±0.31* 6.72±0.30* 5.58±0.28* 5.11±0.27* 5.73±0.27 7.91±0.23* 5.72±0.21 4.58±0.22* 4.11±0.23*
ryegrass shoot 4.62±0.31 3.81±0.21* 3.67±0.24* 3.65±0.22* 3.58±0.21* 4.62±0.31 3.88±0.25* 3.87±0.21* 3.95±0.32* 3.91±0.24*
root 5.68±0.37 6.45±0.36* 4.75±0.29* 4.40±0.30* 4.17±0.31* 5.68±0.37 5.98±0.33* 5.73±0.21 5.37±0.31 5.11±0.27*
radish shoot 0.59±0.01 0.55±0.01* 0.58±0.01 0.69±0.02* 0.85±0.01* 0.59±0.01 0.59±0.02 0.68±0.01* 0.71±0.02* 0.87±0.02*
root 1.12±0.04 1.21±0.03* 1.10±0.03 1.04±0.04 1.23±0.03* 1.12±0.04 1.27±0.03* 1.32±0.12* 1.35±0.03* 1.92±0.03*
cucumber shoot 3.03±0.26 3.32±0.22 3.28±0.27 3.34±0.19 3.49±0.31* 3.03±0.26 3.21±0.12 3.52±0.22* 3.44±0.15* 3.53±0.21*
root 2.56±0.22 2.62±0.21 2.69±0.33 2.72±0.27* 2.71±0.31* 2.56±0.22 2.67±0.11 2.76±0.24* 2.79±0.21* 2.89±0.25*
oat shoot 0.93±0.02 0.99±0.03* 1.03±0.02* 1.09±0.02* 1.18±0.03* 0.93±0.02 1.09±0.02* 1.15±0.02* 1.12±0.02* 1.21±0.02*
root 1.28±0.05 1.31±0.06 1.33±0.05 1.42±0.03* 1.43±0.04* 1.28±0.05 1.39±0.06* 1.41±0.05* 1.45±0.03* 1.48±0.04*
common onion shoot 1.22±0.03 1.26±0.02 0.73±0.03* 0.78±0.018 0.94±0.02* 1.22±0.03 1.59±0.01* 0.98±0.02* 0.82±0.03* 0.97±0.02*
root 1.58±0.02 1.56±0.02 1.21±0.02* 1.37±0.02* 1.59±0.03* 1.58±0.02 1.59±0.01 1.38±0.02* 1.58±0.02 1.64±0.02*
Tab.3  MDA contents of seven test plant species in DnBP or DEHP treatments after germination a)
Fig.1  Mean plant pigment (chlorophyll a+b and carotinoid) contents in alfalfa a), radish b) and onion c) exposed to DnBP or DEHP at 0, 5, 20, 100 and 500?mg·kg−1 after germination for 72?h (168?h for onion). Each point is the mean of three replicates. Bars are standard error of the mean (SEM). Columns with asterisks indicate significant difference at p<0.05 compared with CK
1 N Scholz. Ecotoxicity and biodegradation of phthalate monoesters. Chemosphere, 2003, 53(8): 921–926
https://doi.org/10.1016/S0045-6535(03)00668-4 pmid: 14505714
2 W L Liu, C F Shen, Z Zhang, C B Zhang. Distribution of phthalate esters in soil of e-waste recycling sites from Taizhou city in China. Bulletin of Environmental Contamination and Toxicology, 2009, 82(6): 665–667
https://doi.org/10.1007/s00128-009-9699-3 pmid: 19290451
3 F Zeng, K Y Cui, Z Y Xie, L N Wu, D L Luo, L X Chen, Y J Lin, M Liu, G X Sun. Distribution of phthalate esters in urban soils of subtropical city, Guangzhou, China. Journal of Hazardous Materials, 2009, 164(2–3): 1171–1178
https://doi.org/10.1016/j.jhazmat.2008.09.029 pmid: 18963455
4 J Vikelsøe, M Thomsen, L Carlsen. Phthalates and nonylphenols in profiles of differently dressed soils. Science of the Total Environment, 2002, 296(1–3): 105–116
https://doi.org/10.1016/S0048-9697(02)00063-3 pmid: 12398330
5 R Gibson, M J Wang, E Padgett, A J Beck. Analysis of 4-nonylphenols, phthalates, and polychlorinated biphenyls in soils and biosolids. Chemosphere, 2005, 61(9): 1336–1344
https://doi.org/10.1016/j.chemosphere.2005.03.072 pmid: 15979687
6 X X Hu, Z H Han, B Y Liu, F B Zhang, F Li, W H Wang. Distribution of phthalic acid esters in environment and its toxicity. Environmental Science and Management, 2007, 32(1): 37–40
7 D Schowanek, R Carr, H David, P Douben, J Hall, H Kirchmann, L Patria, P Sequi, S Smith, S Webb. A risk-based methodology for deriving quality standards for organic contaminants in sewage sludge for use in agriculture—Conceptual Framework. Regulatory Toxicology and Pharmacology, 2004, 40(3): 227–251
https://doi.org/10.1016/j.yrtph.2004.07.002 pmid: 15546678
8 L W Chang, J R Meier, M K Smith. Application of plant and earthworm bioassays to evaluate remediation of a lead-contaminated soil. Archives of Environmental Contamination and Toxicology, 1997, 32(2): 166–171
https://doi.org/10.1007/s002449900170 pmid: 9069192
9 Q An, W Jin, Y Li, R W Xu. Influence of plasticizer PAEs to the soil-plant system. Acta Pedologica Sinica, 1999, 2(1): 118–126 (in Chinese)
10 R Yin, X G Lin, S G Wang, H Y Zhang. Influence of phthalic acid esters in vegetable garden soil on quality of capsicum fruit. Agro-Environmental Protection, 2002, 21(1): 1–4 (in Chinese)
11 C S Liao, J H Yen, Y S Wang. Growth inhibition in Chinese cabbage (Brassica rapa var. chinensis) growth exposed to di-n-butyl phthalate. Journal of Hazardous Materials, 2009, 163(2–3): 625– 631
https://doi.org/10.1016/j.jhazmat.2008.07.025 pmid: 18678443
12 US Environmental Protection Agency. 1996. Ecological Effects Test Guidelines (OPPTS 850.4200): Seed Germination / Root Elongation Toxicity Test.
13 X D Wang, C Sun, S X Gao, L S Wang, H Shuokui. Validation of germination rate and root elongation as indicator to assess phytotoxicity with Cucumis sativus. Chemosphere, 2001, 44(8): 1711–1721
https://doi.org/10.1016/S0045-6535(00)00520-8 pmid: 11534903
14 C G Zhang, K K Leung, Y S Wong, N F Y Tam. Germination, growthand physiological responses of mangrove plant (Bruguiera gymnorrhiza) to lubricating oil pollution. Environmental and Experimental Botany, 2007, 60(1): 127–136
https://doi.org/10.1016/j.envexpbot.2006.09.002
15 H K Lichtenthaler, A R Wellburn. Determination of total carotenoids and chlorophyls a and b of leaf extracts in different solvents. Biochemical Society Transactions, 1983, 603(11): 591–592
16 W Wang, P H Keturi. Comparative seed germination tests using ten plant species for toxicity assessment of metals engraving effluent sample. Water, Air, and Soil Pollution, 1990, 52(3–4): 369–376
https://doi.org/10.1007/BF00229444
17 H A Kordan. Seed viability and germination: a multi-purpose experimental system. Journal of Biological Education, 1992, 26(4): 247–251
https://doi.org/10.1080/00219266.1992.9655281
18 M T Moore, D B Huggett, G M Huddleston III, J H Rodgers Jr, C M Cooper. Herbicide effects on Typha latifolia (Linneaus) germination and root and shoot development. Chemosphere, 1999, 38(15): 3637–3647
https://doi.org/10.1016/S0045-6535(98)00561-X
19 O Munzuroglu, H Geckil. Effects of metals on seed germination, root elongation, and coleoptile and hypocotyl growth in Triticum aestivum and Cucumis sativus. Archives of Environmental Contamination and Toxicology, 2002, 43(2): 203–213
https://doi.org/10.1007/s00244-002-1116-4 pmid: 12115046
20 M R Murata, P S Hammes, G E Zharare. Effect of solution pH and calcium concentration on germination and early growth of groundnut. Journal of Plant Nutrition, 2003, 26(6): 1247–1262
https://doi.org/10.1081/PLN-120020368
21 D H Lin, B S Xing. Phytotoxicity of nanoparticles: inhibition of seed germination and root growth. Environmental Pollution, 2007, 150(2): 243–250
https://doi.org/10.1016/j.envpol.2007.01.016 pmid: 17374428
22 Z Zheng, P J He, L M Shao, D J Lee. Phthalic acid esters in dissolved fractions of landfill leachates. Water Research, 2007, 41(20): 4696–4702
https://doi.org/10.1016/j.watres.2007.06.040 pmid: 17631939
23 X R Xu, X Y Li. Adsorption behavior of dibutyl phthalate on marine sediments. Marine Pollution Bulletin, 2008, 57(6–12): 430–408
24 K Shiota, M J Chou, H Nishimura. Embryotoxic effects of di-2-ethylhexyl phthalate (DEHP) and di-n-buty phthalate (DBP) in mice. Environmental Research, 1980, 22(1): 245–253
https://doi.org/10.1016/0013-9351(80)90136-X pmid: 7418682
25 D L Defoe, G W Holcombe, D E Hammermeister, K E Biesinger. Solubility and toxicity of eight phthalate esters to four aquatic organisms. Environmental Toxicology and Chemistry, 1990, 9(5): 623–636
https://doi.org/10.1002/etc.5620090509
26 C A Staples, W J Adams, T F Parkerton, J W Gorsuch, G R Biddinger, K H Reinert. Aquatic toxicity of eighteen phthalate esters. Environmental Toxicology and Chemistry, 1997, 16(5): 875–891
https://doi.org/10.1002/etc.5620160507
27 P Roslev, K Vorkamp, J Aarup, K Frederiksen, P H Nielsen. Degradation of phthalate esters in an activated sludge wastewater treatment plant. Water Research, 2007, 41(5): 969–976
https://doi.org/10.1016/j.watres.2006.11.049 pmid: 17258263
28 Y Liu, Y T Guan, Z H Yang, Z H Cai, T Mizuno, H Tsuno, W P Zhu, X H Zhang. Toxicity of seven phthalate esters to embryonic development of the abalone Haliotis diversicolor supertexta. Ecotoxicology (London, England), 2009, 18(3): 293–303
https://doi.org/10.1007/s10646-008-0283-0 pmid: 19030987
29 C Santibáñez, C Verdugo, R Ginocchio. Phytostabilization of copper mine tailings with biosolids: implications for metal uptake and productivity of Lolium perenne. Science of the Total Environment, 2008, 395(1): 1–10
https://doi.org/10.1016/j.scitotenv.2007.12.033 pmid: 18342913
30 K B Story. Oxidative stress: animal adaptations in nature. Brazilian Journal of Medical and Biological Research, 2006, 29(12): 1715–1733
31 G J Jones, P D Nichols, B Johns, J D Smith. The effect of mercury and cadmiumon the fatty acid and sterol composition of the marine diatom Asterionella glacialis. Phytochemistry, 1987, 26(5): 1343–1348
https://doi.org/10.1016/S0031-9422(00)81809-9
32 M Gupta, S Sinha, P Chandra. Copper-induced toxicity in aquatic macrophyte, Hydrilla verticillata: effect of pH. Ecotoxicology (London, England), 1996, 5(1): 23–33
https://doi.org/10.1007/BF00116321 pmid: 24193506
33 S Singh, S Eapen, S F D’Souza. Cadmium accumulation and its influence on lipid peroxidation and antioxidative system in an aquatic plant, Bacopa monnieri L. Chemosphere, 2006, 62(2): 233–246
https://doi.org/10.1016/j.chemosphere.2005.05.017 pmid: 15993469
34 T J Zou, T X Li, X Z Zhang, H Y Yu, H B Luo. Lead accumulation and tolerance characteristics of Athyrium wardii (Hook.) as a potential phytostabilizer. Journal of Hazardous Materials, 2011, 186(1): 683–689
https://doi.org/10.1016/j.jhazmat.2010.11.053 pmid: 21144654
35 S H Wang, Z M Yang, B Lu, S Q Li, Y P Lu. Copper induced stress and antioxidative responses in roots of Brassica juncea L. Botanical Bulletin of Academia Sinica, 2004, 45: 203–212 (in Chinese)
36 N H Song, X L Yin, G F Chen, H Yang. Biological responses of wheat (Triticum aestivum) plants to the herbicide chlorotoluron in soils. Chemosphere, 2007, 68(9): 1779–1787
https://doi.org/10.1016/j.chemosphere.2007.03.023 pmid: 17462703
37 J Fábregas, A Domínguez, D G Álvarez, T Lamela, A Otero. García álvarez D, Lamela T, Otero A. Induction of astaxanthin accumulation by nitrogen and magnesium deficiencies in Haematococcus pluvialis. Biotechnology Letters, 1998, 20(6): 623–626
https://doi.org/10.1023/A:1005322416796
38 R Mascher, B Lippmann, S Holzinger, H Bergmann. Arsenate toxicity: effects on oxidative stress response molecules and enzymes in red clover plants. Plant Science, 2002, 163(5): 961–969
https://doi.org/10.1016/S0168-9452(02)00245-5
39 A Lagriffoul, B Mocquot, M Mench, J Vangronsveld. Cadmium toxicity effects on growth, mineral and chlorophyll contents, and activities of stress related enzymes in young maize plants (Zea mays L.). Plant and Soil, 1998, 200(2): 241–250
https://doi.org/10.1023/A:1004346905592
40 P J Ralph. Herbicide toxicity of Halophila ovalis assessed by chlorophyll a fluorescence. Aquatic Botany, 2000, 66(2): 141–152
https://doi.org/10.1016/S0304-3770(99)00024-8
41 S Sinha, R Saxena, S Singh. Comparative studies on accumulation of Cr from metal solution and tannery effluent under repeated metal exposure by aquatic plants: its toxic effects. Environmental Monitoring and Assessment, 2002, 80(1): 17–31
https://doi.org/10.1023/A:1020357427074 pmid: 12437061
42 M Aslan, M Y Unlü, N Türkmen, Y Z Yilmaz. Sorption of cadmium and effects on growth, protein content, and photosynthetic pigment composition of Nasturtium officinale R. Br. and Mentha aquatica L. Bulletin of Environmental Contamination and Toxicology, 2003, 71(2): 323–329
https://doi.org/10.1007/s00128-003-0167-1 pmid: 14560384
43 V Vange, I Heuch, V Vandvik. Do seed mass and family affect germination and juvenile performance in Knautia arvensis? A study using failure-time methods. Acta Oecologica, 2004, 25(3): 169–178
https://doi.org/10.1016/j.actao.2004.01.002
44 R W Dolan. The effect of seed size and maternal source on individual size in a population of Ludwigia leptocarpa (Onagraceae). American Journal of Botany, 1984, 71(9): 1302–1307
https://doi.org/10.2307/2443655
45 M L Stanton. Seed variation in wild radish: effect of seed size on components of seedling and adult fitness. Ecology, 1984, 65(4): 1105–1112
https://doi.org/10.2307/1938318
46 A A Winn. Ecological and evolutionary consequences of seed size in Prunella vulgaris. Ecology, 1988, 69(5): 1537–1544
https://doi.org/10.2307/1941651
47 C Houssard, J Escarré. The effects of seed weight on growth and competitive ability of Rumex acetosella from two successional oldfields. Oecologia, 1991, 86(2): 236–242
https://doi.org/10.1007/BF00317536
48 A M Simons, M O Johnston. Variation in seed traits of Lobelia inflata (Campanulaceae): sources and fitness consequences. American Journal of Botany, 2000, 87(1): 124–132
https://doi.org/10.2307/2656690 pmid: 10636835
49 R D Wulff. Seed size variation in Desmodium paniculatum. II. Effects on seedling growth and physiological performance. Journal of Ecology, 1986, 74(1): 99–114
https://doi.org/10.2307/2260351
50 G Vaughton, M Ramsey. Relationships between seed mass, seed nutrients, and seedling growth in Banksia cunninghamii (Proteaceae). International Journal of Plant Sciences, 2001, 162(3): 599–606
https://doi.org/10.1086/320133
51 N C George, J E Sands. The control of seed germination by moisture as a soil physical property. Australian Journal of Agricultural Research, 1959, 10(5): 628–636
https://doi.org/10.1071/AR9590628
52 D Come. Obstacles to germination. Monographies de Physiologie Vegetale, 1970, 6: 162
53 B K Takemoto, R D Noble. Differential sensitivity of duckweeds (Lemnaceae) to sulphite. I. Carbon assimilation and frond replication rate as factors influencing sulphite phytotoxicity under low and high irradiance. New Phytologist, 1986, 103(3): 525–539
https://doi.org/10.1111/j.1469-8137.1986.tb02890.x
54 B Ait, J C Audran. Response of champenoise grapevine to low temperatures: Changes of shoot and bud proline concentrations in response to low temperatures and correlations with freezing tolerance. Journal of Horticultural Science, 1987, 72(4): 577–582
55 O Blokhina, E Virolainen, K V Fagerstedt. Antioxidants, oxidative damage and oxygen deprivation stress: a review. Annals of Botany, 2003, 91(2 Spec No): 179–194
https://doi.org/10.1093/aob/mcf118 pmid: 12509339
56 N A Shaharuddin, F Kawamura, O Sulaiman, R Hashim. Evaluation on antioxidant activity, antifungal activity and total phenolic of selected commercial Malaysian timbers. In: Proceedings of International Conference on Environmental Research and Technology. Penang Malaysia: Press of the National University of Malaysia, 2008, 970–974
57 M M Posmyk, R Kontek, K M Janas. Antioxidant enzymes activity and phenolic compounds content in red cabbage seedlings exposed to copper stress. Ecotoxicology and Environmental Safety, 2009, 72(2): 596–602
https://doi.org/10.1016/j.ecoenv.2008.04.024 pmid: 18801573
58 C Sgherri, E Cosi, F Navari-Izzo. Phenols and antioxidative status of Raphanus sativus grown in copper excess. Plant Physiology, 2003, 118(1): 21–28
https://doi.org/10.1034/j.1399-3054.2003.00068.x pmid: 12702010
59 N Terry. Limiting factors in photosynthesis. 1. Use of iron stress to control photochemical capacity in vivo. Plant Physiology, 1980, 65(1): 114–120
https://doi.org/10.1104/pp.65.1.114 pmid: 16661123
60 J A Manthey, D E Crowley. Leaf and root responses to iron deficiency in avocado. Journal of Plant Nutrition, 1997, 20(1): 683–693
https://doi.org/10.1080/01904169709365286
Viewed
Full text


Abstract

Cited

  Shared   
  Discussed