Effects of complex saline-alkali stress on seed germination and seedling antioxidant characteristics of Chenopodium quinoa

doi:10.11686/cyxb2018181

Abstract

Abstract: The saline-alkali conditions in many parts of Northern China constitute a soil factor causing significant restrictions to quinoa development. In order to better understand the adaptive physiology of quinoa under saline-alkali stress, this research focused on quinoa seed germination, antioxidant enzyme activities and isozyme characteristics. A set of 20 different alkali-saline plant stress conditions were simulated by mixing two neutral (NaCl and Na₂SO₄) and alkaline (NaHCO₃ and Na₂CO₃) salts with soil in different proportions (A, NaCl∶Na₂SO₄=1∶1. B, NaCl∶Na₂SO₄∶ NaHCO₃=1∶2∶1. C, NaCl∶Na₂SO₄∶NaHCO₃∶Na₂CO₃=1∶9∶9∶1. D, NaCl∶Na₂SO₄∶NaHCO₃∶Na₂CO₃=1∶1∶1∶1. E, NaCl∶Na₂SO₄∶NaHCO₃∶Na₂CO₃=9∶1∶1∶9) and at concentrations of (50, 100, 150 and 200 mmol·L^-1). Several germination and physiological indices, such as the germination percentage, germination index, germination energy were measured, and the activities of SOD, POD, CAT and GR were also analysed, and isoenzymic zymograms prepared. It was found that the five different saline-alkali stress formulations all decreased quinoa germination percentage, germination index and germination energy. With increasing saline-alkali concentration, germination was decreased dramatically (P<0.05). Compared to the control, saline-alkali stress induced higher activities of SOD and GR under treatments A and B, and lower activity of SOD under treatments C, D, and E, while GR activity was significantly increased at 50 mmol·L^-1 salt concentration. The activity of POD was the highest when the concentration of saline-alkali solution was 50 mmol·L^-1; with increased salt concentration, POD activity fell to levels 4 times lower than control, and CAT activity also decreased. SDS-PAGE revealed that saline-alkali stress induced significant changes to isomer ratios of antioxidant enzymes (SOD, POD, CAT, GR), including new isoforms. These results indicate that salt-alkaline stress inhibited seed germination of quinoa. For Na₂SO₄ and NaHCO₃ on the germination inhibition of quinoa seeds was more obvious. The threshold of salt tolerance was 50 mmol·L^-1 in this study, and salt concentration was the main determinant of the degree of inhibition, with the composition of the salt solution being a minor factor.

Key words: Chenopodium quinoa, saline-alkali stress, seed germination, anti-oxidative enzymes, enzyme isoform

ZHAO Ying, WEI Xiao-hong, HE Ya-long, ZHAO Xiao-fei, HAN Ting, YUE Kai, XIN Xia-qing, SU Mei-fei, MA Wen-jing, LUO Qiao-juan. Effects of complex saline-alkali stress on seed germination and seedling antioxidant characteristics of Chenopodium quinoa[J]. Acta Prataculturae Sinica, 2019, 28(2): 156-167.

References

[1] Wang L M, Ma N, Li S, et al. Nutritional properties of quinoa and its application prospects. Science and Technology of Food Industry, 2014, 35(1): 381-384, 389.
王黎明, 马宁, 李颂, 等. 藜麦的营养价值及其应用前景. 食品工业科技, 2014, 35(1): 381-384, 389.
[2] Jacobsen S E, Mujica A, Jensen C R.The resistance of quinoa (Chenopodium quinoa Willd.) to adverse abiotic factors. Food Reviews International, 2003, 19(1/2): 99-109.
[3] Wilson C, Read J J, Abo- Kassem E.Effect of mixed-salt salinity on growth and ion relations of a quinoa and a wheat variety. Journal of Plant Nutrition, 2002, 25(12): 2689-2704.
[4] Jacobsen S E, Liu F, Jensen C R.Does root-sourced ABA play a role for regulation of stomata under drought in quinoa (Chenopodium quinoa Willd.). Scientia Horticulturae, 2009, 122(2): 281-287.
[5] Raney J A, Reynolds D J, Elzinga D B, et al. Transcriptome analysis of drought induced stress in Chenopodium quinoa. American Journal of Plant Sciences, 2014, 5(3): 338-357.
[6] Jacobsen S E, Monteros C, Christiansen J L, et al. Plant responses of quinoa (Chenopodium quinoa Willd.) to frost at various phenological stages. European Journal of Agronomy, 2005, 22(2): 131-139.
[7] Gu X, Huang J, Wei Y M, et al. Development prospect and research progress of Chenopodium quinoa. Chinese Agricultural Science Bulletin, 2015, 31(30): 201-204.
顾娴, 黄杰, 魏玉明, 等. 藜麦研究进展及发展前景. 中国农学通报, 2015, 31(30): 201-204.
[8] Wang C J, Zhao X W, Lu G O, et al. A review of characteristics and utilization of Chenopodium quinoa. Journal of Zhejiang Agricultural and Forestry University, 2014, 31(2): 296-301.
王晨静, 赵习武, 陆国权, 等. 藜麦特性及开发利用研究进展. 浙江农林大学学报, 2014, 31(2): 296-301.
[9] Yu Z Y, Liang S M.Analysis of irrigation water using efficiency in arid and semi-arid areas in northwest China based on Miami model. Journal of Arid Land Resource and Environment, 2017, 31(9): 49-55.
于智媛, 梁书民. 基于Miami模型的西北干旱半干旱地区灌溉用水效果评价——以甘宁蒙为例. 干旱区资源与环境, 2017, 31(9): 49-55.
[10] Chang R Q, Wang L X, Li X P.Soil nutrition barriers in the southern area of ningxia. Agricultural Research in the Arid Areas, 1997, 15(2): 63-68.
常庆瑞, 王立祥, 李新平. 宁南地区土壤营养障碍性分析. 干旱地区农业研究, 1997, 15(2): 63-68.
[11] Liu W Y, Yang F R, Huang J, et al. Response of seedling growth and the activity of antioxidant enzymes of Chenopodium quinoato salt stress. Acta Botanica Boreali-Occidentalia Sinica, 2017, 37(9): 1797-1804.
刘文瑜, 杨发荣, 黄杰, 等. NaCl胁迫对藜麦幼苗生长和抗氧化酶活性的影响. 西北植物学报, 2017, 37(9): 1797-1804.
[12] Yang H W, Liu W Y, Shen B Y, et al. Seed germination and physiological characteristics of Chenopodium quinoa under salt stress. Acta Prataculturae Sinica, 2017, 26(8): 146-153.
杨宏伟, 刘文瑜, 沈宝云, 等. NaCl胁迫对藜麦种子萌发和幼苗生理特性的影响. 草业学报, 2017, 26(8): 146-153.
[13] Zhang Z W, Pang C H, Zhang Y Q, et al. Effect of iso-osmotic NaCl and PEG stress and rewatering on seed germination and seedling growth of quinoa. Crops, 2017, (1): 119-126.
张紫薇, 庞春花, 张永清, 等. 等渗NaCl和PEG胁迫及复水处理对藜麦种子萌发及幼苗生长的影响. 作物杂志, 2017, (1): 119-126.
[14] Shabala L, Mackay A, Tian Y, et al. Oxidative stress protection and stomatal patterning as components of salinity tolerance mechanism in quinoa (Chenopodium quinoa). Physiologia Plantarum, 2012, 146(1): 26-38.
[15] Adolf V I, Jacobsen S E, Shabala S.Salt tolerance mechanisms in quinoa (Chenopodium quinoa Willd). Environmental & Experimental Botany, 2013, 92: 43-54.
[16] Han D H, Zhang Y, Jin L.Effects of basic salt and mixed salt-alkali stress tolerance on seed germination and seedling physiological characteristic of Astraglus membranaceus var. mongholicus. Chinese Traditional and Herbal Drugs, 2013, 43(12): 1661-1666.
韩多红, 张勇, 晋玲. 碱性盐及混合盐碱胁迫对蒙古黄芪种子萌发和幼苗生理特性的影响. 中草药, 2013, 43(12): 1661-1666.
[17] Li R, Shi F, Fukuda K.Interactive effects of various salt and alkali stresses on growth, organic solutes, and cation accumulation in a halophyte Spartina alterniflora (Poaceae). Environmental and Experimental Botany, 2010, 68(1): 66-74.
[18] Zhang X L, Liu X J, Qi M X, et al. Alfalfa seeding root characteristics under complex saline-alkali stress. Chinese Journal of Eco-Agricultural, 2013, 21(3): 340-346.
张晓磊, 刘晓静, 齐敏兴, 等. 混合盐碱对紫花苜蓿苗期根系特征的影响. 中国生态农业学报, 2013, 21(3): 340-346.
[19] Song J, Feng G, Zhang F S.Salinity and temperature effects on germination for three salt-resistant euhalophytes, Halostachys caspica, Kalidium foliatum and Halocnemum strobilaceum. Plant and Soil, 2006, 279(1/2): 201-207.
[20] Song J, Feng G, Tian C Y, et al. Strategies for adaptation of Suaeda physophora, Haloxylon ammodendron and Haloxylon persicum to a saline environment during seed germination stage. Annals of Botany, 2005, 96(1): 399-405.
[21] Gulnar Yasin, Yang R R, Zeng Y L.Effects of salt-alkali mixed stresses on seed germination of the halophyte Chenopodium glaucum L. Chinese Journal of Ecology, 2014, 33(1): 76-82.
古丽内尔·亚森, 杨瑞瑞, 曾幼玲. 混合盐碱胁迫对灰绿藜(Chenopodium glaucum L.)种子萌发的影响. 生态学杂志, 2014, 33(1): 76-82.
[22] Li B B, Wei X H, Hu Y.The causes of Gentiana straminea Maxim. seeds dormancy and the methods for its breaking. Acta Ecologica Sinica, 2013, 33(15): 4631-4638.
李兵兵,魏小红,徐严. 麻花秦艽种子休眠机制及破除方法. 生态学报, 2013, 33(15): 4631-4638
[23] Liu W Y, Yang H W, Wei X H, et al. Effect of exogenous nitric oxide on seed germination, physiological characteristics and active oxygen metabolism of Medicago truncatula under NaCl stress. Acta Prataculturae Sinaca, 2015, 24(2): 85-95.
刘文瑜, 杨宏伟, 魏小红, 等. 外源NO调控盐胁迫下蒺藜苜蓿种子萌发生理特性及抗氧化酶的研究. 草业学报, 2015, 24(2): 85-95.
[24] Shi J, Fu X Z, Peng T, et al. Spermine pretreatment confers dehydration tolerance of citrus in vitro plants via modylation of antioxidative capacity and stomatal response. Tree Phusuology, 2010, 30(7): 914-922.
[25] Chen J X, Wang X F.Guide of plant physiological experiments. Guangzhou: South China University of Technology Press, 2006.
陈建勋, 王晓峰. 植物生理学实验指导. 广州: 华南理工大学出版社, 2006.
[26] Halliwell B, Foyer C H.Properties and physiological function of a glutathione reductase purified from spinach leaves by affinity chromatography. Planta, 1978, 139(16): 9-17.
[27] Hu N S, Wan X G.Isoenzyme technology and its application. Changsha: Hunan Science and Technology Press, 1985: 3-105.
胡能书, 万贤国. 同工酶技术及其应用. 长沙: 湖南科学技术出版社, 1985: 3-105.
[28] Liang H W, Liu S, Chen F J, et al. Changes of peroxidase and esterase isoenzymes in the process of germination of silver magpie trees. Seed, 2006, 25(5): 38-40.
梁宏伟, 刘姝, 陈发菊, 等. 银鹊树种子萌发过程中的过氧化物酶和酯酶同工酶的变化.种子, 2006, 25(5): 38-40.
[29] Aravind P, Varaprasad M N.Modulation of cadmium-induced oxidative stress in Ceratophyllum demersum by zinc involves ascorbate-glutathione cycle and glutathione metabolism. Plant physiology and Biochemistry, 2005, 43(2): 107-116.
[30] Shen Z B, Pan D F, Wang J L, et al. Effects of saline-alkaloid stress on seed germination and seedling growth of grass. Acta Agrestia Sinica, 2012, 20(5): 914-920.
申忠宝, 潘多峰, 王建丽, 等. 混合盐碱胁迫对5种禾草种子萌发及幼苗生长的影响. 草地学报, 2012, 20(5): 914-920.
[31] Zhang Y, Han D H, Jin L, et al. Effects of different salt-alkaline stress on seed germination and physiological characteristics of Hedysarum polybotrys. China Journal of Chinese Materia Medica, 2012, 37(20): 3036-3040.
张勇, 韩多红, 晋玲, 等. 不同盐碱胁迫对红芪种子萌发和幼苗生理特性的影响. 中国中药杂志, 2012, 37(20): 3036-3040.
[32] Xu T J, Dong Z Q, Lan H L, et al. Effects of PASP-KT-NAA on photosynthesis and antioxidant enzyme activities of maize seedlings under low temperature stress. Acta agronomica sinica, 2012, 38(2):352-359.
徐田军, 董志强, 兰洪亮, 等. 低温胁迫下聚糠萘合剂对玉米幼苗光合作用和抗氧化酶活性的影响. 作物学报, 2012, 38(2): 352-359.
[33] Tan S D, Zhu M Y, Dang H S, et al. Physiological response of bermudagrass (Cynodon dactylon L. Pers) to deep submergence stress in the three gorges reservoir area. Acta Ecologica Sinica, 2009, 29(7): 3685-3691.
谭淑端, 朱明勇, 党海山, 等. 三峡库区狗牙根对深淹胁迫的生理响应. 生态学报, 2009, 29(7): 3685-3691.
[34] Zhang M, Liu J, Yang Z M, et al. Effects of high temperature stress on the activities and isozymes of antioxidant enzymes in kentucky bluegrass. Acta Agrestia sinica, 2014, 22(6): 1308-1317.
张梅, 刘君, 杨志民, 等. 高温胁迫对草地早熟禾抗氧化酶活性及其同工酶图谱的影响.草地学报, 2014, 22(6): 1308-1317.
[35] Bai J H.The physiological mechanisms of oat responding to salt and alkali stress. Hohhot: Inner Mongolia Agricultural University, 2016.
白健慧. 燕麦对盐碱胁迫的生理响应机制研究. 呼和浩特: 内蒙古农业大学, 2016.
[36] Chowdhury M A, Slinkard A E.Genetic diversity in grasspea (Lathyrus sativus L.). Genetic Resources and Crop Evolution, 2000, 47(2): 163-169.
[37] Toyomasu T, Zennyoxi A.On the application of isoenzyme electrophoresis to identification of strains in Leurinus edodes. Mushroom Science, 1981, 11: 675-684.
[38] Liu C J, Chao S, Gale M D.The genetical control of tissue-specific peroxidases, per-1, per-2, per-3, per-4, and per-5 in wheat. Theoretical and Applied Genetics, 1990, 79(3): 305-313.
[39] Sun J, Wang X Z.Effects of salts stress on gene expression of peroxidase isozyme in wheat. Journal of Triticeae Crops, 2006, 42-44.
孙静, 王宪泽. 盐胁迫对小麦过氧化物酶同工酶基因表达的影响. 麦类作物学报, 2006, 26(1): 42-44.
[40] Guo L H, Chen S N, Wang D B, et al. Changes in activity of glutathione reductase and it’s isozyme of maize seedlings during heat shock and heat stress. Journal of Yunnan University. 2006, 28(3): 262-266.
郭丽红, 陈善娜, 王德斌, 等. 热激和热胁迫过程中玉米幼苗谷胱甘肽还原酶活性和同工酶的变化. 云南大学学报, 2006, 262-266.
[41] Wang W X, Wang X F, Yan Q H.Changes of antioxidant enzymes during salt stress on seedling leaves of tomato (Lycopersicon esculentum L.). Journal of Sichuan Agricultural University, 2013, 31(2): 169-175.
王维香, 汪晓峰, 严庆海. 盐胁迫对番茄幼苗(Lycopersicon esculentum L.)抗氧化酶活性和同工酶的影响. 四川农业大学学报, 2013, 31(2): 169-175.
[42] Zhao F Y, Hu F, Han M M, et al. Relationship between H₂O₂ and changes of glutathione reductase activity and isoenzyme pattern induced by stress. Acta Botanica Boreali-Occidentalia Sinica, 2011, 31(3): 543-551.
赵凤云, 胡凡, 韩明明, 等. 胁迫诱导谷胱甘肽还原酶活性和同工酶谱的变化与H₂O₂的关系. 西北植物学报, 2011, 31(3): 543-551.