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Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

Physiological response in the leaf and stolon of white clover under acid precipitation and freeze–thaw stress

Guozhang Bao https://orcid.org/0000-0003-0329-8001 A D , Wenyi Tang A , Fanglin He A , Weiwei Chen A , Yue Zhu A , Cunxin Fan B , Mengyu Zhang A , Yixin Chang A , Jiaxing Sun A and Xuemei Ding C
+ Author Affiliations
- Author Affiliations

A Key Laboratory of Groundwater Resources and Environment of the Ministry of Education, College of New Energy and Environment, Jilin University, Changchun 130023, China.

B The Administration of Jingyu Water Conservation, Jingyu, Jilin Province 135200, China.

C College of Animal Science, Jilin University, Changchun 130023, China.

D Corresponding author. Email: baogz@jlu.edu.cn

Functional Plant Biology 47(1) 50-57 https://doi.org/10.1071/FP19072
Submitted: 14 March 2019  Accepted: 30 August 2019   Published: 9 December 2019

Abstract

Freeze–thaw (FT) in northern China is a common event in spring and autumn, and the release of sulfur dioxide from coal-burning in winter is apt to trigger acid precipitation. Both these stresses can aggravate the wintering ability of white clover (Trifolium repens L.). Acid precipitation and FT simulation experiments were carried out in the field and an indoor alternation refrigerator, respectively. The contents of soluble protein, soluble sugar, malondialdehyde (MDA), proline and antioxidant activity were tested under acid precipitation and FT stress. The results showed that under acid precipitation stress, the content of MDA, peroxidase and superoxide dismutase increased in both leaves and stolons, whereas soluble protein and soluble sugar content declined compared with the control groups. During the freezing period, the content of antioxidant enzyme activity, soluble protein and proline increased at first and then dropped, whereas MDA and soluble sugar content both increased. As a conclusion, the stolon of white clover is more sensitive than the leaf to short-term stress, either as the single FT stress or the combined stress of FT and acid precipitation, suggesting that maintaining more leaves can contribute to the resistance of white clover to these stresses.

Additional keywords: antioxidant enzymes, osmoregulation, Trifolium repens.


References

Baek KH, Skinner DZ (2003) Alteration of antioxidant enzyme gene expression during cold acclimation of near-isogenic wheat lines. Plant Science 165, 1221–1227.
Alteration of antioxidant enzyme gene expression during cold acclimation of near-isogenic wheat lines.Crossref | GoogleScholarGoogle Scholar |

Bao GZ, Ao Q, Li QQ, Bao YS, Zheng Y, Feng XX, Ding XM (2017) Physiological characteristics of Medicago sativa L. in response to acid deposition and freeze–thaw stress. Water, Air, and Soil Pollution 228, 376
Physiological characteristics of Medicago sativa L. in response to acid deposition and freeze–thaw stress.Crossref | GoogleScholarGoogle Scholar |

Bellani LM, Rinallo C, Muccifora S, Gori P (1997) Effects of simulated acid rain on pollen physiology and ultrastructure in the apple. Environmental Pollution 95, 357–362.
Effects of simulated acid rain on pollen physiology and ultrastructure in the apple.Crossref | GoogleScholarGoogle Scholar | 15093450PubMed |

Bian WJ, Bao GZ, Qian HM, Song ZW, Qi ZM, Zhang MY, Chen WW, Dong WY (2018) Physiological response characteristics in Medicago sativa under freeze–thaw and deicing salt stress. Water, Air, and Soil Pollution 229, 196–203.
Physiological response characteristics in Medicago sativa under freeze–thaw and deicing salt stress.Crossref | GoogleScholarGoogle Scholar |

Bini C, Bresolin F (1998) Soil acidification by acid rain in forest ecosystems: a case study in northern Italy. The Science of the Total Environment 222, 1–15.
Soil acidification by acid rain in forest ecosystems: a case study in northern Italy.Crossref | GoogleScholarGoogle Scholar |

Chapin III FS, Matson PA, Vitousek PM (2002) ‘Principles of terrestrial ecosystem ecology.’ (Springer-Verlag: New York)

Chen YP, Zhang J, Yang ZJ, Yu F, Li YQ (2012) Relationship between nitric oxide accumulation, anti-oxidative system and freezing tolerance in the leaves of Sabina during cold adaptation. Journal of Animal and Plant Sciences 22, 1133–1141.

Chen J, Wang WH, Liu TW, Wu FH, Zheng HL (2013) Photosynthetic and antioxidant responses of Liquidambar formosana and Schima superba seedlings to sulfuric-rich and nitric-rich simulated acid rain. Plant Physiology and Biochemistry 64, 41–51.
Photosynthetic and antioxidant responses of Liquidambar formosana and Schima superba seedlings to sulfuric-rich and nitric-rich simulated acid rain.Crossref | GoogleScholarGoogle Scholar | 23353765PubMed |

Desikan R, Mackerness SAH, Hancock JT, Neill SJ (2001) Regulation of the Arabidopsis transcriptome by oxidative stress. Plant Physiology 127, 159–172.
Regulation of the Arabidopsis transcriptome by oxidative stress.Crossref | GoogleScholarGoogle Scholar | 11553744PubMed |

Dolatabadian A, Sanavy SAMM, Gholamhoseini M, Joghan AK, Majdi M, Kashkooli AB (2013) The role of calcium in improving photosynthesis and related physiological and biochemical attributes of spring wheat subjected to simulated acid rain. Physiology and Molecular Biology of Plants 19, 189–198.
The role of calcium in improving photosynthesis and related physiological and biochemical attributes of spring wheat subjected to simulated acid rain.Crossref | GoogleScholarGoogle Scholar | 24431486PubMed |

Feng ZW, Miao H, Zhang FZ, Huang YZ (2002) Effects of acid deposition on terrestrial ecosystems and their rehabilitation strategies in China. Journal of Environmental Sciences (China) 14, 227–233.

Fitzhugh RD, Driscoll CT, Groffman PM, Tierney GL, Fahey TJ, Hardy JP (2001) Effects of soil freezing on soil solution nitrogen, phosphorus, and carbon chemistry in a northern hardwood ecosystem. Biogeochemistry 56, 215–238.
Effects of soil freezing on soil solution nitrogen, phosphorus, and carbon chemistry in a northern hardwood ecosystem.Crossref | GoogleScholarGoogle Scholar |

Fleck RA, Day JG, Clarke KJ, Benson EE (1999) Elucidation of the metabolic and structural basis for the cryopreservation recalcitrance of Vaucheria sessilis. Cryo Letters 20, 271–282.

Guo FX, Zhang MX, Chen Y, Zhang WH, Xu SJ, Wang JH, An LZ (2006) Relation of several antioxidant enzymes to rapid freezing resistance in suspension cultured cells from alpine Chorispora bungeana. Cryobiology 52, 241–250.
Relation of several antioxidant enzymes to rapid freezing resistance in suspension cultured cells from alpine Chorispora bungeana.Crossref | GoogleScholarGoogle Scholar | 16426599PubMed |

Guy CL (2003) Freezing tolerance of plants: current understanding and selected emerging concepts. Canadian Journal of Botany 81, 1216–1223.
Freezing tolerance of plants: current understanding and selected emerging concepts.Crossref | GoogleScholarGoogle Scholar |

Høgh-Jensen H, Schjoerring JK (2001) Rhizodeposition of nitrogen by red clover, white clover and ryegrass leys. Soil Biology & Biochemistry 33, 439–448.
Rhizodeposition of nitrogen by red clover, white clover and ryegrass leys.Crossref | GoogleScholarGoogle Scholar |

Hu YC (2014) Study on the influence of simulated acid rain on clover. Anhui Nongye Kexue 42, 85–89. [In Chinese]

Hu J, Xie XJ, Wang ZF, Song WJ (2006) Sand priming improves alfalfa germination under high-salt concentration stress. Seed Science and Technology 34, 199–204.
Sand priming improves alfalfa germination under high-salt concentration stress.Crossref | GoogleScholarGoogle Scholar |

Jones PD, Moberg A (2003) Hemispheric and large-scale surface air temperature variations: an extensive revision and an update to 2001. Journal of Climate 16, 206–223.
Hemispheric and large-scale surface air temperature variations: an extensive revision and an update to 2001.Crossref | GoogleScholarGoogle Scholar |

Kacharava N, Chkhubianishvili E, Badridze G (2013) Antioxidant response of some Georgian wheat species to simulated acid rain. Australian Journal of Crop Science 7, 770–776.

Kang JP, Zhen N, Bai R (2011) Study on evaluation of turf use value of wild Trifolium repens in Greater Khingan Range, Inner Mongolia Science & Technology and Economy 14, 62–64. [In Chinese]

Kita I, Sato T, Kase Y, Mitropoulos P (2004) Neutral rains at Athens, Greece: a natural safeguard against acidification of rains. Science of the Total Environment 327, 285–294.
Neutral rains at Athens, Greece: a natural safeguard against acidification of rains.Crossref | GoogleScholarGoogle Scholar | 15172587PubMed |

Larssen T, Lydersen E, Tang DG, He Y, Gao JX, Liu HY, Duan L, Seip HM, Vogt RD, Mulder J, Shao M, Wang YH, Shang H, Zhang XS, Solberg S, Aas W, Okland T, Eilertsen O, Angell V, Liu QR, Zhao DW, Xiang RJ, Xiao JS, Luo JH (2006) Acid rain in China. Environmental Science & Technology 40, 418–425.
Acid rain in China.Crossref | GoogleScholarGoogle Scholar |

Li JP, Xu CB, Zhao LX, Wang Y, Zhao HX (2009) Progress of biotechnology in white clover. Shengwu Jishu Tongbao 5, 39–42. [In Chinese]

Liu EU, Liu CP (2011) Effects of simulated acid rain on the antioxidative system in Cinnamomum philippinense seedlings. Water, Air, and Soil Pollution 215, 127–135.
Effects of simulated acid rain on the antioxidative system in Cinnamomum philippinense seedlings.Crossref | GoogleScholarGoogle Scholar |

Liu BS, Kang CL, Wang X, Bao GZ (2015a) Tolerance mechanisms of Leymus chinensis to salt–alkaline stress. Acta Agriculturæ Scandinavica. Section B, Soil and Plant Science 65, 723–734.
Tolerance mechanisms of Leymus chinensis to salt–alkaline stress.Crossref | GoogleScholarGoogle Scholar |

Liu BS, Kang CL, Wang X, Bao GZ (2015b) Physiological and morphological responses of Leymus chinensis to saline–alkali stress. Grassland Science 61, 217–226.
Physiological and morphological responses of Leymus chinensis to saline–alkali stress.Crossref | GoogleScholarGoogle Scholar |

Montillet JL, Chamnongpol S, Rusterucci C, Dat J, van de Cotte B, Agnel JP, Battesti C, Inze D, Van Breusegem F, Triantaphylides C (2005) Fatty acid hydroperoxides and H2O2 in the execution of hypersensitive cell death in tobacco leaves. Plant Physiology 138, 1516–1526.
Fatty acid hydroperoxides and H2O2 in the execution of hypersensitive cell death in tobacco leaves.Crossref | GoogleScholarGoogle Scholar | 15980200PubMed |

Ren XQ, Zhu JZ, Liu HY, Xu X, Liang CJ (2018) Response of antioxidative system in rice (Oryza sativa) leaves to simulated acid rain stress. Ecotoxicology and Environmental Safety 148, 851–856.
Response of antioxidative system in rice (Oryza sativa) leaves to simulated acid rain stress.Crossref | GoogleScholarGoogle Scholar |

Shi Q, Bao Z, Zhu Z, Ying Q, Qian Q (2006) Effects of different treatments of salicylic acid on heat tolerance, chlorophyll fluorescence, and antioxidant enzyme activity in seedlings of Cucumis sativa L. Plant Growth Regulation 48, 127–135.
Effects of different treatments of salicylic acid on heat tolerance, chlorophyll fluorescence, and antioxidant enzyme activity in seedlings of Cucumis sativa L.Crossref | GoogleScholarGoogle Scholar |

Shukla JB, Sundar S, Shivangi , Naresh R (2013) Modeling and analysis of the acid rain formation due to precipitation and its effect on plant species. Natural Resource Modeling 26, 53–65.
Modeling and analysis of the acid rain formation due to precipitation and its effect on plant species.Crossref | GoogleScholarGoogle Scholar |

Si Y, Wang LH, Zhou Q, Huang XH (2018) Effects of lanthanum and acid rain stress on the bio-sequestration of lanthanum in phytoliths in germinated rice seeds. PLoS One 13, e0197365
Effects of lanthanum and acid rain stress on the bio-sequestration of lanthanum in phytoliths in germinated rice seeds.Crossref | GoogleScholarGoogle Scholar | 30566461PubMed |

Singh A, Agrawal M (2008) Acid rain and its ecological consequences. Journal of Environmental Biology 29, 15–24.

Valentovič P, Luxová M, Kolarovič L, Gašparíková O (2006) Effect of osmotic stress on compatible solutes content, membrane stability and water relations in two maize cultivars. Plant, Soil and Environment 52, 186–191.
Effect of osmotic stress on compatible solutes content, membrane stability and water relations in two maize cultivars.Crossref | GoogleScholarGoogle Scholar |

Wen KJ, Liang CJ, Wang LH, Hu G, Zhou Q (2011) Combined effects of lanthanumion and acid rain on growth, photosynthesis and chloroplast ultrastructure in soybean seedlings. Chemosphere 84, 601–608.
Combined effects of lanthanumion and acid rain on growth, photosynthesis and chloroplast ultrastructure in soybean seedlings.Crossref | GoogleScholarGoogle Scholar |

Wu FX, Luo MS, Wang WL, Wu BJ (2013) Distribution characteristics of acid rain in Jilin Province. Environmental Science & Technology 36, 187–191. [In Chinese]

Xu SF, Wu XH, Cai YQ, Ding YK, Wang Z (2018) Strength and leaching characteristics of magnesium phosphate cement-solidified zinc-contaminated soil under the effect of acid rain. Soil & Sediment Contamination 27, 161–174.
Strength and leaching characteristics of magnesium phosphate cement-solidified zinc-contaminated soil under the effect of acid rain.Crossref | GoogleScholarGoogle Scholar |

Yan QJ, Cai J, Li Y, Liu ZB (2016) The different physiological responses of natural and stationary low temperature on white clover (Trifolium repens L.). In ‘Advances in engineering research. Vol. 67’. (Eds B Ma, D Zhou) pp. 482–489. (Atlantis Press, Paris)

Zhang Y, He J, Zhao PX, Bouton JH, Monteros MJ (2008) Genome-wide identification of microsatellites in white clover (Trifolium repens L.) using FIASCO and phpSSRMiner. Plant Methods 4, 9

Zhou RL, Zhao HL (2004) Seasonal pattern of antioxidant enzyme system in the roots of perennial forage grasses grown in alpine habitat, related to freezing tolerance. Physiologia Plantarum 121, 399–408.
Seasonal pattern of antioxidant enzyme system in the roots of perennial forage grasses grown in alpine habitat, related to freezing tolerance.Crossref | GoogleScholarGoogle Scholar |

Zhu XZ, Huang Y, Yang XZ (2009) Effects of simulated acid rain on decomposition of soil organic carbon and crop straw. Journal of Applied Ecology 20, 480–484.