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RESEARCH ARTICLE

Physiological changes associated with enhanced cold resistance during maize (Zea mays) germination and seedling growth in response to exogenous calcium

Qian Zhang https://orcid.org/0000-0001-5405-8679 A , Yongxi Liu A , Qiaoqiao Yu A , Yue Ma A , Wanrong Gu A and Deguang Yang A B
+ Author Affiliations
- Author Affiliations

A Northeast Agricultural University, College of Agriculture, Harbin 150030, Heilongjiang, China.

B Corresponding author. Email: ydgl@tom.com

Crop and Pasture Science 71(6) 529-538 https://doi.org/10.1071/CP19510
Submitted: 5 December 2019  Accepted: 30 April 2020   Published: 11 June 2020

Abstract

Maize (Zea mays L.) is one of the most important crops worldwide. However, low temperature limits seed germination and seedling growth of maize, which can in turn affect grain yield. The calcium ion (Ca2+) is the second messenger involved in the response to environmental-stimuli-induced signal transduction networks. The underlying physiological mechanisms related to the effects of exogenous Ca2+ treatment of different maize cultivars under low temperature are unclear. We selected two inbred lines, cold-sensitive cv. C546 and cold-tolerant cv. Y478, for studying the effects of Ca2+ on seed germination, photosynthesis, antioxidant enzymes and the osmotic regulation of seedling resistance to low temperature. The optimal concentration of CaCl2 was 80 mmol L–1, which significantly improved the germination percentage at temperatures <10°C. Application of CaCl2 at this concentration under cold stress mitigated the degree of membrane injury and improved the antioxidant enzyme system through reduced relative electrolyte conductivity and malondialdehyde content, increased the soluble protein content, and enhanced superoxide dismutase and peroxidase activity. CaCl2 also significantly increased chlorophyll fluorescence indicators (Fv/Fo, Fv/Fm) and the photosynthetic rate. We conclude that exogenous CaCl2 at a concentration of 80 mmol L–1 protects the function and structure of the membrane and photosystems, improves antioxidant enzyme activity and increases osmotic regulatory substances under cold stress. These results improve our understanding of the mechanisms of Ca2+ and contribute to the development of cold-tolerant maize varieties.

Additional keywords: inbred line, MDA, photosynthetic characteristics.


References

Ahmad P, Jaleel CA, Salem MA, Nabi G, Sharma S (2010) Roles of enzymatic and nonenzymatic antioxidants in plants during abiotic stress. Critical Reviews in Biotechnology 30, 161–175.
Roles of enzymatic and nonenzymatic antioxidants in plants during abiotic stress.Crossref | GoogleScholarGoogle Scholar | 20214435PubMed |

Annunziata MG, Ciarmiello LF, Woodrow P, Aversana ED, Carillo P (2019) Spatial and temporal profile of glycine betaine accumulation in plants under abiotic stresses. Frontiers in Plant Science 10,
Spatial and temporal profile of glycine betaine accumulation in plants under abiotic stresses.Crossref | GoogleScholarGoogle Scholar | 30899269PubMed |

Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annual Review of Plant Biology 55, 373–399.
Reactive oxygen species: metabolism, oxidative stress, and signal transduction.Crossref | GoogleScholarGoogle Scholar | 15377225PubMed |

Aroca R, Porcel R, Ruiz-Lozano JM (2012) Regulation of root water uptake under abiotic stress conditions. Journal of Experimental Botany 63, 43–57.
Regulation of root water uptake under abiotic stress conditions.Crossref | GoogleScholarGoogle Scholar | 21914658PubMed |

Ashraf M, Harris PJC (2013) Photosynthesis under stressful environments: an overview. Photosynthetica 51, 163–190.

Baker NR, Rosenqvist E (2004) Applications of chlorophyll fluorescence can improve crop production strategies, an examination of future possibilities. Journal of Experimental Botany 55, 1607–1621.
Applications of chlorophyll fluorescence can improve crop production strategies, an examination of future possibilities.Crossref | GoogleScholarGoogle Scholar | 15258166PubMed |

Barlow PW, Pilet PE (1983) Mitotic activity in the maize root apex after freeze-decapping. Planta 157, 286–288.
Mitotic activity in the maize root apex after freeze-decapping.Crossref | GoogleScholarGoogle Scholar | 24264161PubMed |

Chen Y, Jiang J, Chang Q, Gu C, Song A, Chen F (2014) Cold acclimation induces freezing tolerance via antioxidative enzymes, proline metabolism and gene expression changes in two chrysanthemum species. Molecular Biology Reports 41, 815–822.
Cold acclimation induces freezing tolerance via antioxidative enzymes, proline metabolism and gene expression changes in two chrysanthemum species.Crossref | GoogleScholarGoogle Scholar | 24413987PubMed |

Chinnusamy V, Zhu J, Zhu JK (2007) Cold stress regulation of gene expression in plants. Trends in Plant Science 12, 444–451.
Cold stress regulation of gene expression in plants.Crossref | GoogleScholarGoogle Scholar | 17855156PubMed |

Corpas FJ, Barroso JB, del Río LA (2001) Peroxisomes as a source of reactive oxygen species and nitric oxide signal molecules in plant cells. Trends in Plant Science 6, 145–150.
Peroxisomes as a source of reactive oxygen species and nitric oxide signal molecules in plant cells.Crossref | GoogleScholarGoogle Scholar | 11286918PubMed |

Cutforth HW, Shaykewich CF, Cho CM (1986) Effect of soil water and temperature on corn (Zea mays L.) root growth during emergence. Canadian Journal of Soil Science 66, 51–58.

Frascaroli E, Landi P (2017) Registration of maize inbred line Bo23 with high cold tolerance and agronomic performance for early sowing. Journal of Plant Registrations 11, 172–177.
Registration of maize inbred line Bo23 with high cold tolerance and agronomic performance for early sowing.Crossref | GoogleScholarGoogle Scholar |

Galon Y, Finkler A, Fromm H (2010) Calcium-regulated transcription in plants. Molecular Plant 3, 653–669.
Calcium-regulated transcription in plants.Crossref | GoogleScholarGoogle Scholar | 20457642PubMed |

Giannopolitis CN, Ries SK (1977) Superoxide dismutases: I. Occurrence in higher plants. Plant Physiology 59, 309–314.
Superoxide dismutases: I. Occurrence in higher plants.Crossref | GoogleScholarGoogle Scholar | 16659839PubMed |

Hajiboland R, Aliasgharzadeh N, Laiegh SF, Poschenrieder C (2010) Colonization with arbuscular mycorrhizal fungi improves salinity tolerance of tomato (Solanum lycopersicum L.) plants. Plant and Soil 331, 313–327.
Colonization with arbuscular mycorrhizal fungi improves salinity tolerance of tomato (Solanum lycopersicum L.) plants.Crossref | GoogleScholarGoogle Scholar |

Hansen J, Sato M, Ruedy R, Lacis A, Oinas V (2000) Global warming in the twenty-first century: an alternative scenario. Proceedings of the National Academy of Sciences of the United States of America 97, 9875–9880.
Global warming in the twenty-first century: an alternative scenario.Crossref | GoogleScholarGoogle Scholar | 10944197PubMed |

Heath RL, Packer L (1968) Photo peroxidation in isolated chloroplasts: I. Kinetics and stoichiometry of fatty acid peroxidation. Archives of Biochemistry and Biophysics 125, 189–198.
Photo peroxidation in isolated chloroplasts: I. Kinetics and stoichiometry of fatty acid peroxidation.Crossref | GoogleScholarGoogle Scholar | 5655425PubMed |

Hernández JA, Jiménez A, Mullineaux P, Sevilla F (2000) Tolerance of pea (Pisum sativum L.) to long-term salt stress is associated with induction of antioxidant defenses. Plant, Cell & Environment 23, 853–862.
Tolerance of pea (Pisum sativum L.) to long-term salt stress is associated with induction of antioxidant defenses.Crossref | GoogleScholarGoogle Scholar |

Huang XS, Wang W, Zhang Q, Liu JH (2013) A basic helix-loop-helix transcription factor, PtrbHLH, of Poncirus trifoliata confers cold tolerance and modulates peroxidase-mediated scavenging of hydrogen peroxide. Plant Physiology 162, 1178–1194.
A basic helix-loop-helix transcription factor, PtrbHLH, of Poncirus trifoliata confers cold tolerance and modulates peroxidase-mediated scavenging of hydrogen peroxide.Crossref | GoogleScholarGoogle Scholar | 23624854PubMed |

Huang D, Gong X, Liu Y, Zeng G, Lai C, Bashir H, Zhou L, Wang D, Xu P, Cheng M, Wan J (2017) Effects of calcium at toxic concentrations of cadmium in plants. Planta 245, 863–873.
Effects of calcium at toxic concentrations of cadmium in plants.Crossref | GoogleScholarGoogle Scholar | 28204874PubMed |

Kazemi-Shahandashti SS, Maali-Amiri R, Zeinali H, Khazaei M, Talei A, Ramezanpour SS (2014) Effect of short-term cold stress on oxidative damage and transcript accumulation of defense-related genes in chickpea seedlings. Journal of Plant Physiology 171, 1106–1116.
Effect of short-term cold stress on oxidative damage and transcript accumulation of defense-related genes in chickpea seedlings.Crossref | GoogleScholarGoogle Scholar | 24972025PubMed |

Knight H, Knight MR (2000) Imaging spatial and cellular characteristics of low temperature calcium signature after cold acclimation in Arabidopsis. Journal of Experimental Botany 51, 1679–1686.
Imaging spatial and cellular characteristics of low temperature calcium signature after cold acclimation in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 11053457PubMed |

Knight H, Trewavas AJ, Knight MR (1996) Cold calcium signaling in Arabidopsis involves two cellular pools and a change in calcium signature after acclimation. The Plant Cell 8, 489–503.

Kudla J, Batistic O, Hashimoto K (2010) Calcium signals: the lead currency of plant information processing. The Plant Cell 22, 541–563.
Calcium signals: the lead currency of plant information processing.Crossref | GoogleScholarGoogle Scholar | 20354197PubMed |

Lei P, Xu Z, Ding Y, Tang B, Zhang Y, Li H, Feng X, Xu H (2015) Effect of poly (γ-glutamic acid) on the physiological responses and calcium signaling of rape seedlings (Brassica napus L.) under cold stress. Journal of Agricultural and Food Chemistry 63, 10399–10406.
Effect of poly (γ-glutamic acid) on the physiological responses and calcium signaling of rape seedlings (Brassica napus L.) under cold stress.Crossref | GoogleScholarGoogle Scholar | 26585291PubMed |

Lei P, Xu Z, Ji L, Luo X, Zhang Y, Feng X, Xu H (2016) Poly (γ-glutamic acid) enhanced tolerance to salt stress by promoting proline accumulation in Brassica napus L. Plant Growth Regulation 78, 233–241.
Poly (γ-glutamic acid) enhanced tolerance to salt stress by promoting proline accumulation in Brassica napus L.Crossref | GoogleScholarGoogle Scholar |

Lei P, Pang X, Feng X, Li S, Chi B, Wang R, Xu Z, Xu H (2017) The microbe-secreted isopeptide poly-γ-glutamic acid induces stress tolerance in Brassica napus L. seedlings by activating crosstalk between H2O2 and Ca2+. Scientific Reports 7, 41618
The microbe-secreted isopeptide poly-γ-glutamic acid induces stress tolerance in Brassica napus L. seedlings by activating crosstalk between H2O2 and Ca2+.Crossref | GoogleScholarGoogle Scholar | 28198821PubMed |

Li LJ, Gu WR, Ji L, Li CF, Xie TL, Qu DY, Meng Y, Wei S (2018) Exogenously applied spermidine alleviates photosynthetic inhibition under drought stress in maize (Zea mays L.) seedlings associated with changes in endogenous polyamines and phytohormones. Plant Physiology and Biochemistry 129, 35–55.
Exogenously applied spermidine alleviates photosynthetic inhibition under drought stress in maize (Zea mays L.) seedlings associated with changes in endogenous polyamines and phytohormones.Crossref | GoogleScholarGoogle Scholar |

Li M, Lin L, Zhang Y, Sui N (2019) ZmMYB31, a R2R3-MYB transcription factor in maize, positively regulates the expression of CBF genes and enhances resistance to chilling and oxidative stress. Molecular Biology Reports 46, 3937–3944.
ZmMYB31, a R2R3-MYB transcription factor in maize, positively regulates the expression of CBF genes and enhances resistance to chilling and oxidative stress.Crossref | GoogleScholarGoogle Scholar | 31037550PubMed |

Manimaran P, Mangrauthia SK, Sundaram RM, Balachandran SM (2015) Constitutive expression and silencing of a novel seed specific calcium dependent protein kinase gene in rice reveals its role in grain filling. Journal of Plant Physiology 174, 41–48.
Constitutive expression and silencing of a novel seed specific calcium dependent protein kinase gene in rice reveals its role in grain filling.Crossref | GoogleScholarGoogle Scholar | 25462965PubMed |

Matschi S, Werner S, Schulze WX, Legen J, Hilger HH, Romeis T (2013) Function of calcium-dependent protein kinase CPK28 of Arabidopsis thaliana in plant stem elongation and vascular development. The Plant Journal 73, 883–896.
Function of calcium-dependent protein kinase CPK28 of Arabidopsis thaliana in plant stem elongation and vascular development.Crossref | GoogleScholarGoogle Scholar | 23252373PubMed |

Maxwell K, Johnson GN (2000) Chlorophyll fluorescence—a practical guide. Journal of Experimental Botany 51, 659–668.
Chlorophyll fluorescence—a practical guide.Crossref | GoogleScholarGoogle Scholar | 10938857PubMed |

Moradtalab N, Weinmann M, Walker F, Höglinger B, Ludewig U, Neumann G (2018) Silicon improves chilling tolerance during early growth of maize by effects on micronutrient homeostasis and hormonal balances. Frontiers in Plant Science 9, 420
Silicon improves chilling tolerance during early growth of maize by effects on micronutrient homeostasis and hormonal balances.Crossref | GoogleScholarGoogle Scholar | 29755482PubMed |

Muñoz BG, Lekfeldt JDS, Magid J, Jensen LS, De Neergaard A (2018) Seed treatment with Penicillium sp. or Mn/Zn can alleviate the negative effects of cold stress in maize grown in soils dependent on soil fertility. Journal of Agronomy and Crop Science 204, 603–612.

National Bureau of Statistics of China (2012) ‘China statistics yearbook.’ (China Statistics Press: Beijing)

Pandey GK, Cheong YH, Kim KN, Grant JJ, Li L, Hung W, D’Angelo C, Weinl S, Kudla J, Luan S (2004) The calcium sensor calcineurin B-like 9 modulates abscisic acid sensitivity and biosynthesis in Arabidopsis. The Plant Cell 16, 1912–1924.
The calcium sensor calcineurin B-like 9 modulates abscisic acid sensitivity and biosynthesis in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 15208400PubMed |

Ray S, Agarwal P, Arora R, Kapoor S, Tyagi AK (2007) Expression analysis of calcium-dependent protein kinase gene family during reproductive development and abiotic stress conditions in rice (Oryza sativa L. ssp. indica). Molecular Genetics and Genomics 278, 493–505.
Expression analysis of calcium-dependent protein kinase gene family during reproductive development and abiotic stress conditions in rice (Oryza sativa L. ssp. indica).Crossref | GoogleScholarGoogle Scholar | 17636330PubMed |

Rentel MC, Knight MR (2004) Oxidative stress-induced calcium signaling in Arabidopsis. Plant Physiology 135, 1471–1479.
Oxidative stress-induced calcium signaling in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 15247375PubMed |

Rosenwasser S, Fluhr R, Joshi JR, Leviatan N, Sela N, Hetzroni A, Friedman H (2013) ROSMETER: a bioinformatic tool for the identification of transcriptomic imprints related to reactive oxygen species type and origin provides new insights into stress responses. Plant Physiology 163, 1071–1083.
ROSMETER: a bioinformatic tool for the identification of transcriptomic imprints related to reactive oxygen species type and origin provides new insights into stress responses.Crossref | GoogleScholarGoogle Scholar | 23922270PubMed |

Rymen B, Fiorani F, Kartal F, Vandepoele K, Inzé D, Beemster GTS (2007) Cold nights impair leaf growth and cell cycle progression in maize through transcriptional changes of cell cycle genes. Plant Physiology 143, 1429–1438.
Cold nights impair leaf growth and cell cycle progression in maize through transcriptional changes of cell cycle genes.Crossref | GoogleScholarGoogle Scholar | 17208957PubMed |

Sharkey TD, Zhang R (2010) High temperature effects on electron and proton circuits of photosynthesis. Journal of Integrative Plant Biology 52, 712–722.
High temperature effects on electron and proton circuits of photosynthesis.Crossref | GoogleScholarGoogle Scholar | 20666927PubMed |

Shi H, Ye T, Zhong B, Liu X, Chan Z (2014) Comparative proteomic and metabolomic analyses reveal mechanisms of improved cold stress tolerance in bermudagrass (Cynodon dactylon (L.) Pers.) by exogenous calcium. Journal of Integrative Plant Biology 56, 1064–1079.
Comparative proteomic and metabolomic analyses reveal mechanisms of improved cold stress tolerance in bermudagrass (Cynodon dactylon (L.) Pers.) by exogenous calcium.Crossref | GoogleScholarGoogle Scholar | 24428341PubMed |

Singh I, Kumar U, Singh SK, Gupta C, Singh M, Kushwaha SR (2012) Physiological and biochemical effect of 24-epibrassinoslide on cold tolerance in maize seedlings. Physiology and Molecular Biology of Plants 18, 229–236.

Verheul MJ, Picatto C, Stamp P (1996) Growth and development of maize (Zea mays L.) seedlings under chilling conditions in the field. European Journal of Agronomy 5, 31–43.
Growth and development of maize (Zea mays L.) seedlings under chilling conditions in the field.Crossref | GoogleScholarGoogle Scholar |

Wang Y, Gu W, Xie T, Li L, Sun Y, Zhang H, Wei S (2016) Mixed compound of DCPTA and CCC increases maize yield by improving plant morphology and up-regulating photosynthetic capacity and antioxidants. PLoS One 11, e0149404
Mixed compound of DCPTA and CCC increases maize yield by improving plant morphology and up-regulating photosynthetic capacity and antioxidants.Crossref | GoogleScholarGoogle Scholar | 28036354PubMed |

Wang L, Zhang P, Wang R, Wang P, Huang S (2018a) Effects of variety and chemical regulators on cold tolerance during maize germination. Journal of Integrative Agriculture 17, 2662–2669.
Effects of variety and chemical regulators on cold tolerance during maize germination.Crossref | GoogleScholarGoogle Scholar |

Wang X, Wu L, Xie JJ, Li TH, Cai J, Zhou Q, Dai TB, Jiang D (2018b) Herbicide isoproturon aggravates the damage of low temperature stress and exogenous ascorbic acid alleviates the combined stress in wheat seedlings. Plant Growth Regulation 84, 293–301.
Herbicide isoproturon aggravates the damage of low temperature stress and exogenous ascorbic acid alleviates the combined stress in wheat seedlings.Crossref | GoogleScholarGoogle Scholar |

Wang Y, Li J, Gu W, Zhang Q, Tian L, Guo S, Wei S (2018c) Exogenous application of 5-aminolevulinic acid improves low-temperature stress tolerance of maize seedlings. Crop & Pasture Science 69, 587–593.
Exogenous application of 5-aminolevulinic acid improves low-temperature stress tolerance of maize seedlings.Crossref | GoogleScholarGoogle Scholar |

Whalley HJ, Sargeant AW, Steele JF, Lacoere T, Lamb R, Saunders NJ, Knight H, Knight MR (2011) Transcriptomic analysis reveals calcium regulation of specific promoter motifs in Arabidopsis. The Plant Cell 23, 4079–4095.
Transcriptomic analysis reveals calcium regulation of specific promoter motifs in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 22086087PubMed |

Xu S, Li J, Zhang X, Wei H, Cui L (2006) Effects of heat acclimation pretreatment on changes of membrane lipid peroxidation, antioxidant metabolites, and ultrastructure of chloroplasts in two cool-season turfgrass species under heat stress. Environmental and Experimental Botany 56, 274–285.
Effects of heat acclimation pretreatment on changes of membrane lipid peroxidation, antioxidant metabolites, and ultrastructure of chloroplasts in two cool-season turfgrass species under heat stress.Crossref | GoogleScholarGoogle Scholar |

Zhang Z, Wu P, Zhang W, Yang Z, Liu H, Ahammed GJ, Cui J (2020) Calcium is involved in exogenous NO-induced enhancement of photosynthesis in cucumber (Cucumis sativus L.) seedlings under low temperature. Scientia Horticulturae 261, 108953
Calcium is involved in exogenous NO-induced enhancement of photosynthesis in cucumber (Cucumis sativus L.) seedlings under low temperature.Crossref | GoogleScholarGoogle Scholar |