The effects of exogenous ABA applied to maize (Zea mays L.) roots on plant responses to chilling stress

  • Li-xin Tian
  • Jing Li
Original Article


This work aimed to discuss the effects of exogenous abscisic acid (ABA) on the root growth regulation of maize seedlings under chilling stress. The roots of the maize cultivar Zhengdan 958 were irrigated with ABA (10−7, 10−6, 10−5 and 10−4 M) at the third true leaf stage under chilling duration (0, 2, 4, 6, and 8 days). The biomass, the phenylalanine ammonia lyase (PAL), and polyphenol oxidase (PPO) enzyme activities, total phenolic and flavonoid contents, the ferric reducing ability of plasma (FRAP) antioxidant capacity, and 2,2-azinobis (3-ethlbenzothiazo-line-6-sulfonic acid) diammonium salt radical (ABTS·+) scavenging capacity of the roots of maize seedlings were measured after the treatment. The results showed that appropriate concentrations of exogenous ABA effectively enhanced root biomass, increased PAL and PPO enzyme activities, and significantly increased total phenolic contents and flavonoid contents. Moreover, the ABA markedly improved the FRAP antioxidant capacity and ABTS·+ scavenging capacity under low-temperature stress. These results indicate that ABA-treated maize seedlings are resistant to chilling stress and that the optimum concentration of ABA is 10−5 M. Exogenous applications of ABA have a concentration effect in alleviating chilling stress, in which low concentrations have a promoting effect and high concentrations have an inhibiting effect.


Abscisic acid Maize Chilling Root Physiological characteristics 



This work was funded by the National Key Research and Development (R&D) Program of China (No. 2017YFD0300405).


  1. Adom KK, Sorrells ME, Liu RH (2003) Phytochemical profiles and antioxidant activity of wheat varieties. J Agric Food Chem 51:7825–7834CrossRefPubMedGoogle Scholar
  2. Aghdam MS, Asghari M, Farmani B, Mohayeji M, Moradbeygi H (2012) Impact of postharvest brassinosteroids treatment on PAL activity in tomato fruit in response to chilling stress. Sci Hortic Amst 144:116–120CrossRefGoogle Scholar
  3. Aghdam MS, Jannatizadeh A, Sheikh-Assadi M, Malekzadeh P (2016) Alleviation of postharvest chilling injury in anthurium cut flowers by salicylic acid treatment. Sci Hortic Amst 202:70–76CrossRefGoogle Scholar
  4. Ahmad P, Ahanger MA, Alyemeni MN, Wijaya L, Alam P (2018) Exogenous application of nitric oxide modulates osmolyte metabolism, antioxidants, enzymes of ascorbate-glutathione cycle and promotes growth under cadmium stress in tomato. Protoplasma 255:79–83CrossRefPubMedGoogle Scholar
  5. Assis JS, Maldonado R, Muñoz T, Escribano MI, Merodio C (2001) Effect of high carbon dioxide concentration on PAL activity and phenolic contents in ripening cherimoya fruit. Postharvest Biol Technol 23:33–39CrossRefGoogle Scholar
  6. Bakht J, Bano A, Shafi M, Dominy P (2013) Effect of abscisic acid applications on cold tolerance in chickpea (Cicer arietinum L.). Eur J Agron 44:10–21CrossRefGoogle Scholar
  7. Bate NJ, Orr J, Ni W, Meromi A, Nadlerhassar T, Doerner PW, Dixon RA, Lamb CJ, Elkind Y (1994) Quantitative relationship between phenylalanine ammonia-lyase levels and phenylpropanoid accumulation in transgenic tobacco identifies a rate-determining step in natural product synthesis. Proc Natl Acad Sci USA 91:7608–7612CrossRefPubMedPubMedCentralGoogle Scholar
  8. Benzie IF, Strain JJ (1996) The ferric reducing ability of plasma (FRAP) as a measure of “antioxidant power”: the FRAP assay. Anal Biochem 239:70–76CrossRefPubMedGoogle Scholar
  9. Bortoluzzi EC, Parize GL, Korchagin J, Silva VRD, Rheinheimer DDS, Kaminski J (2014) Soybean root growth and crop yield in response to liming at the beginning of a no-tillage system. Revista Brasileira De Ciência Do Solo 38:262–271CrossRefGoogle Scholar
  10. Branca G (2015) Graft incompatibility in plants: metabolic changes during formation and establishment of the rootstock/scion union with emphasis on Prunus species. Chil J Agric Res 75:20–31Google Scholar
  11. Christie PJ, Alfenito MR, Walbot V (1994) Impact of low-temperature stress on general phenylpropanoid and anthocyanin pathways: enhancement of transcript abundance and anthocyanin pigmentation in maize seedlings. Planta 194:541–549CrossRefGoogle Scholar
  12. Cui JD, Qiu JQ, Fan XW, Jia SR, Tan ZL (2014) Biotechnological production and applications of microbial phenylalanine ammonia lyase: a recent review. Crit Rev Biotechnol 34:258CrossRefPubMedGoogle Scholar
  13. Dumont E, Bahrman N, Goulas E, Valot BT, Sellier H, Hilbert JL, Vuylsteker C, Lejeune-Hénaut I, Delbreil B (2011) A proteomic approach to decipher chilling response from cold acclimation in pea (Pisum sativum L.). Plant Sci 180:86–98CrossRefPubMedGoogle Scholar
  14. Fahimirad S, Karimzadeh G, Ghanati F (2013) Cold-induced changes of antioxidant enzymes activity and lipid peroxidation in two canola (Brassica napus L.) cultivars. J Plant Physiol Br 3:1–11Google Scholar
  15. Farooqi MQ, Sa KJ, Hong TK, Lee JK (2016) Bulk segregant analysis (BSA) for improving cold stress resistance in maize using SSR markers. Genet Mol Res 15:1–12CrossRefGoogle Scholar
  16. Gao H, Kang LN, Liu Q, Ni C, Wang BN, Wei C (2015) Effect of 24-epibrassinolide treatment on the metabolism of eggplant fruits in relation to development of pulp browning under chilling stress. J Food Sci 52:3394–3401Google Scholar
  17. Gao H, Zhang ZK, Lv XG, Cheng N, Peng BZ, Cao W (2016) Effect of 24-epibrassinolide on chilling injury of peach fruit in relation to phenolic and proline metabolisms. Postharvest Biol Technol 111:390–397CrossRefGoogle Scholar
  18. Gould KS, Mckelvie J, Markham KR (2002) Do anthocyanins function as antioxidants in leaves? Imaging of H2O2 in red and green leaves after mechanical injury. Plant Cell Environ 25:1261–1269CrossRefGoogle Scholar
  19. Haberle J, Svoboda P (2015) Calculation of available water supply in crop root zone and the water balance of crops. Contrib Geophys Geod 45:285–298Google Scholar
  20. Heim KE, Tagliaferro AR, Bobilya DJ (2002) Flavonoid antioxidants: chemistry, metabolism and structure–activity relationships. J Nutr Biochem 13:572–584CrossRefPubMedGoogle Scholar
  21. Hsu YT, Kao CH (2003) Role of abscisic acid in cadmium tolerance of rice (Oryza sativa L.) seedlings. Plant Cell Environ 26:867–874CrossRefPubMedGoogle Scholar
  22. Jaleel CA, Sankar B, Murali PV, Gomathinayagam M, Lakshmanan GM, Panneerselvam R (2008) Water deficit stress effects on reactive oxygen metabolism in Catharanthus roseus; impacts on ajmalicine accumulation. Colloid Surf B 62:105–111CrossRefGoogle Scholar
  23. Janowiak F, Dörffling K (1996) Chilling of maize seedlings: changes in water status and abscisic acid content in ten genotypes differing in chilling tolerance. J Plant Physiol 147:582–588CrossRefGoogle Scholar
  24. Jia Z, Tang M, Wu J (1999) The determination of flavonoid contents in mulberry and their scavenging effects on superoxide radicals. Food Chem 64:555–559CrossRefGoogle Scholar
  25. Kadlecová Z, Faltus M, Prášil I (2000) Relationship between abscisic acid content, dry weight and freezing tolerance in barley cv. Lunet. J Plant Physiol 157:291–297CrossRefGoogle Scholar
  26. Karimi R, Ershadi A (2015) Role of exogenous abscisic acid in adapting of ‘Sultana’ grapevine to low-temperature stress. Acta Physiol Plant 37:151CrossRefGoogle Scholar
  27. Kaur L, Zhawar VK (2015) Phenolic parameters under exogenous ABA, water stress, salt stress in two wheat cultivars varying in drought tolerance. Ind J Plant Physiol 20:151–156CrossRefGoogle Scholar
  28. Kumar D, Mishra DS, Chakraborty B, Kumar P (2013) Pericarp browning and quality management of litchi fruit by antioxidants and salicylic acid during ambient storage. J Food Sci Technol 50:797–802CrossRefPubMedGoogle Scholar
  29. Latif F, Ullah F, Mehmood S, Khattak A, Khan AU, Khan S, Husain I (2016) Effects of salicylic acid on growth and accumulation of phenolics in Zea mays L. under drought stress. Acta Agric Scand A 66:325–332Google Scholar
  30. Li XJ, Yang MF, Chen H, Qu LQ, Chen F, Shen SH (2010) Abscisic acid pretreatment enhances salt tolerance of rice seedlings: proteomic evidence. BBA Proteins Proteom 1804:929–940CrossRefGoogle Scholar
  31. Lu S, Su W, Li H, Guo Z (2009) Abscisic acid improves drought tolerance of triploid bermudagrass and involves H2O2- and NO-induced antioxidant enzyme activities. Plant Physiol Biochem 47:132–138CrossRefPubMedGoogle Scholar
  32. Luan LY, Zhang ZW, Xi ZM, Huo SS, Ma LN (2014) Comparing the effects of exogenous abscisic acid on the phenolic composition of Yan 73 and Cabernet Sauvignon (Vitis vinifera L.) wines. Eur Food Res Technol 239:203–213CrossRefGoogle Scholar
  33. Mitchell HJ, Hall JL, Barber MS (1994) Elicitor-induced cinnamyl alcohol dehydrogenase activity in lignifying wheat (Triticum aestivum L.) leaves. Plant Physiol 104:551–556CrossRefPubMedPubMedCentralGoogle Scholar
  34. Murr DP, Morris LL (1974) Influence of O2 and CO2 on o-diphenol oxidase activity in mushrooms. J Am Soc Hortic Sci 99:155–158Google Scholar
  35. Mustafa MA, Ali A, Seymour G, Tucke G (2016) Enhancing the antioxidant content of carambola (Averrhoa carambola) during cold storage and methyl jasmonate treatments. Postharvest Biol Technol 118:79–86CrossRefGoogle Scholar
  36. Naczk M, Shahidi F (2006) Phenolics in cereals, fruits and vegetables: occurrence, extraction and analysis. J Pharm Biomed 41:1523–1542CrossRefGoogle Scholar
  37. Palma F, Carvajal F, Jamilena M, Garrido D (2016) Putrescine treatment increases the antioxidant response and carbohydrate content in zucchini fruit stored at low temperature. Postharvest Biol Technol 118:68–70CrossRefGoogle Scholar
  38. Palta JA, Yang J (2014) Crop root system behaviour and yield. Field Crop Res 165:1–4CrossRefGoogle Scholar
  39. Perveen S, Iqbal M, Parveen A, Akram MS, Shahbaz M, Akber S, Mehboob A (2017) Exogenous triacontanol-mediated increase in phenolics, proline, activity of nitrate reductase, and shoot K+ confers salt tolerance in maize (Zea mays L.). Braz J Bot 40:1–11CrossRefGoogle Scholar
  40. Plaza L, Crespo I, De PS, De AB, Sánchezmoreno C, Muñoz M, Cano MP (2011) Impact of minimal processing on orange bioactive compounds during refrigerated storage. Food Chem 124:646–651CrossRefGoogle Scholar
  41. Potapovich AI, Kostyuk VA (2003) Comparative study of antioxidant properties and cytoprotective activity of flavonoids. Biochemistry 68:514–519PubMedGoogle Scholar
  42. Prior RL, Wu X, Schaich K (2005) Standardized methods for the determination of antioxidant capacity and phenolics in foods and dietary supplements. J Agric Food Chem 53:4290–4302CrossRefPubMedGoogle Scholar
  43. Re R, Pellegrini N, Proteggente A, Pannala A, Yang M, Riceevans C (1999) Antioxidant activity applying an improved ABTS radical cation decolorization assay. Free Radic Biol Med 26:1231–1237CrossRefPubMedGoogle Scholar
  44. Rivero RM, Ruiz JM, Garcia PC, López-Lefebre LR, Sánchez E, Romero L (2001) Resistance to cold and heat stress: accumulation of phenolic compounds in tomato and watermelon plants. Plant Sci 160:315–321CrossRefPubMedGoogle Scholar
  45. Robertson AJ, Mackenzie SL (1994) Abscisic acid-induced heat tolerance in Bromus inermis Leyss cell-suspension cultures. Heat-stable, abscisic acid-responsive polypeptides in combination with sucrose confer enhanced thermostability. Plant Physiol 105:181–190CrossRefPubMedPubMedCentralGoogle Scholar
  46. Salinas-Moreno Y, Lopez-Reynoso JDJ, Gonzalez-Flores GB, Vazquez-Carrillo G (2007) Phenolic compounds of maize grain and their relationship with darkening in dough and tortilla. Agrociencia-Mexico 41:295–305Google Scholar
  47. Sandhu AK, Gray DJ, Lu J, Gu L (2011) Effects of exogenous abscisic acid on antioxidant capacities, anthocyanins, and flavonol contents of muscadine grape (Vitis rotundifolia) skins. Food Chem 126:982–988CrossRefGoogle Scholar
  48. Shen Y, Liang J, Peng X, Yan L, Bao J (2009) Total phenolics, flavonoids, antioxidant capacity in rice grain and their relations to grain color, size and weight. J Cereal Sci 49:106–111CrossRefGoogle Scholar
  49. Siboza XI, Bertling I, Odindo AO (2014) Salicylic acid and methyl jasmonate improve chilling tolerance in cold-stored lemon fruit (Citrus limon). J Plant Physiol 171:1722–1731CrossRefPubMedGoogle Scholar
  50. Singleton VL, Orthofer R, Lamuela-Raventós RM (1999) Analysis of total phenols and other oxidation substrates and antioxidants by means of Folin–Ciocalteu reagent. Method Enzymol 299:152–178CrossRefGoogle Scholar
  51. Song H, Yuan W, Jin P, Wang W, Wang X, Yang L, Zhang Y (2016) Effects of chitosan/nano-silica on postharvest quality and antioxidant capacity of loquat fruit during cold storage. Postharvest Biol Technol 119:41–48CrossRefGoogle Scholar
  52. Stewart RJ, Sawyer BJB, Bucheli CS, Robinson SP, Stewart RJ, Sawyer BJB, Bucheli CS, Robinson SP (2001) Polyphenol oxidase is induced by chilling and wounding in pineapple. Aust J Plant Physiol 28:181–191Google Scholar
  53. Szafrańska K, Szewczyk R, Janas KM (2014) Involvement of melatonin applied to Vigna radiata L. seeds in plant response to chilling stress. Cent Eur J Biol 9:1117–1126Google Scholar
  54. Taşgin E, Atici O, Nalbantoğlu B, Popova LP (2006) Effects of salicylic acid and cold treatments on protein levels and on the activities of antioxidant enzymes in the apoplast of winter wheat leaves. Phytochemistry 67:710–715CrossRefPubMedGoogle Scholar
  55. Wang Y, Luo Z, Huang X, Yang K, Gao S, Du R (2014) Effect of exogenous γ-aminobutyric acid (GABA) treatment on chilling injury and antioxidant capacity in banana peel. Sci Hortic Amst 168:132–137CrossRefGoogle Scholar
  56. Yang L, Yan BX, Yu YM, He XT, Liu QW, Liang ZJ, Yin XW, Cui T, Zhang DX (2016) Global overview of research progress and development of precision maize planters. Int J Agric Biol Eng 9:9–26Google Scholar
  57. Yang Q, Balint-Kurti P, Xu M (2017) Quantitative disease resistance: dissection and adoption in maize. Mol Plant 10:402–413CrossRefPubMedGoogle Scholar
  58. Yeoh WK, Ali A (2017) Ultrasound treatment on phenolic metabolism and antioxidant capacity of fresh-cut pineapple during cold storage. Food Chem 216:247–253CrossRefPubMedGoogle Scholar
  59. Yong SP, Im MH, Choi JH, Lee HC, Ham KS, Kang SG, Park YK, Suhaj M, Namiesnik J, Gorinstein S (2014) Effect of long-term cold storage on physicochemical attributes and bioactive components of kiwi fruit cultivars. Cyta J Food 12:360–368CrossRefGoogle Scholar
  60. Zhang MW, Zhang RF, Zhang FX, Liu RH (2010a) Phenolic profiles and antioxidant activity of black rice bran of different commercially available varieties. J Agric Food Chem 58:7580–7587CrossRefPubMedGoogle Scholar
  61. Zhang ZK, Yu Z, Huber DJ, Rao JP, Sun YJ, Li SS (2010b) Changes in prooxidant and antioxidant enzymes and reduction of chilling injury symptoms during low-temperature storage of ‘Fuyu’ persimmon treated with 1-methylcyclopropene. HortScience 45:1713–1718Google Scholar
  62. Zheng W, Wang SY (2001) Antioxidant activity and phenolic compounds in selected herbs. J Agric Food Chem 49:5165–5170CrossRefPubMedGoogle Scholar
  63. Zhou Z, Robards K, Helliwell S, Blanchard C (2004) The distribution of phenolic acids in rice. Food Chem 87:401–406CrossRefGoogle Scholar
  64. Zhou B, Guo Z, Lin L (2006) Effects of abscisic acid application on photosynthesis and photochemistry of Stylosanthes guianensis under chilling stress. Plant Growth Regul 48:195–199Google Scholar

Copyright information

© Franciszek Górski Institute of Plant Physiology, Polish Academy of Sciences, Kraków 2018

Authors and Affiliations

  1. 1.College of AgronomyNortheast Agricultural UniversityHarbinChina

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