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

Response of waxy maize (Zea mays L. var. ceratina Kulesh) leaf photosynthesis to low temperature during the grain-filling stage

Jian Guo https://orcid.org/0000-0002-6457-1625 A B , Zitao Wang A , Qi Wei A , Guanghao Li A B , Huan Yang A B and Dalei Lu A B C *
+ Author Affiliations
- Author Affiliations

A Jiangsu Key Laboratory of Crop Genetics and Physiology/Jiangsu Key Laboratory of Crop Cultivation and Physiology/Agricultural College, Yangzhou University, Yangzhou 225009, P. R. China.

B Jiangsu Co-Innovation Center for Modern Production Technology of Grain Crops, Yangzhou University, Yangzhou 225009, P. R. China.

C Joint International Research Laboratory of Agriculture and Agri-Product Safety of the Ministry of Education, Yangzhou University, Yangzhou 225009, P. R. China.

* Correspondence to: dllu@yzu.edu.cn

Handling Editor: Suleyman Allakhverdiev

Functional Plant Biology 50(4) 335-346 https://doi.org/10.1071/FP22252
Submitted: 13 October 2022  Accepted: 14 February 2023   Published: 10 March 2023

© 2023 The Author(s) (or their employer(s)). Published by CSIRO Publishing

Abstract

Low temperature (LT) during the grain-filling stage is an important factor that affects the source–sink relationship and leads to yield loss in maize (Zea mays L). In this study, field and pot trials were conducted to investigate the effects of LT during the grain-filling stage on leaf photosynthesis, antioxidant system, hormones, and grain yield of waxy maize cultivars Suyunuo 5 (S5) and Yunuo 7 (Y7). The results showed that LT treatment inhibited the chlorophyll biosynthesis and reduced the photosynthetic pigment levels during grain-filling stage. Ribulose-1,5-bisphosphate carboxylase and phosphoenolpyruvate carboxylase activities, photosynthetic rate, transpiration rate, and stomatal conductance decreased under LT treatment during the grain-filling stage. Furthermore, LT treatment increased the contents of malondialdehyde and reactive oxygen species, and decreased the activities of catalase, superoxide dismutase, peroxidase, and ascorbate peroxidase in the ear leaves, which accelerated the oxidative damage of leaf. The LT treatment also raised abscisic acid content and reduced indole acetic acid content in the ear leaves during grain-filling stage. The results of field and pot trials were verified by each other, but the field effect was greater than that of pot. Overall, LT treatment reduced the waxy maize dry matter accumulation after silking by affecting the physiological and biochemical processes of leaves, and ultimately decreased grain yield.

Keywords: antioxidant enzymes, chlorophyll, endogenous hormones, gas exchange, grain yield, low temperature, photosynthetic enzymes, waxy maize.


References

Ali I, Tang L, Dai J, Kang M, Mahmood A, Wang W, Liu B, Liu L, Cao W, Zhu Y (2021) Responses of grain yield and yield related parameters to post-heading low-temperature stress in Japonica rice. Plants 10, 1425
Responses of grain yield and yield related parameters to post-heading low-temperature stress in Japonica rice.Crossref | GoogleScholarGoogle Scholar |

Amin B, Atif MJ, Wang X, Meng H, Ghani MI, Ali M, Ding Y, Li X, Cheng Z (2021) Effect of low temperature and high humidity stress on physiology of cucumber at different leaf stages. Plant Biology 23, 785–796.
Effect of low temperature and high humidity stress on physiology of cucumber at different leaf stages.Crossref | GoogleScholarGoogle Scholar |

Augspurger CK (2013) Reconstructing patterns of temperature, phenology, and frost damage over 124 years: spring damage risk is increasing. Ecology 94, 41–50.
Reconstructing patterns of temperature, phenology, and frost damage over 124 years: spring damage risk is increasing.Crossref | GoogleScholarGoogle Scholar |

Burnett AC, Kromdijk J (2022) Can we improve the chilling tolerance of maize photosynthesis through breeding? Journal of Experimental Botany 73, 3138–3156.
Can we improve the chilling tolerance of maize photosynthesis through breeding?Crossref | GoogleScholarGoogle Scholar |

Crosatti C, Rizza F, Badeck FW, Mazzucotelli E, Cattivelli L (2013) Harden the chloroplast to protect the plant. Physiologia Plantarum 147, 55–63.
Harden the chloroplast to protect the plant.Crossref | GoogleScholarGoogle Scholar |

de Freitas GM, Thomas J, Liyanage R, Lay JO, Basu S, Ramegowda V, do Amaral MN, Benitez LC, Bolacel Braga EJ, Pereira A (2019) Cold tolerance response mechanisms revealed through comparative analysis of gene and protein expression in multiple rice genotypes. PLoS ONE 14, e0218019
Cold tolerance response mechanisms revealed through comparative analysis of gene and protein expression in multiple rice genotypes.Crossref | GoogleScholarGoogle Scholar |

Dias MC, Brüggemann W (2007) Differential inhibition of photosynthesis under drought stress in Flaveria species with different degrees of development of the C4 syndrome. Photosynthetica 45, 75–84.
Differential inhibition of photosynthesis under drought stress in Flaveria species with different degrees of development of the C4 syndrome.Crossref | GoogleScholarGoogle Scholar |

Dong L, Qi X, Zhu J, Liu C, Zhang X, Cheng B, Mao L, Xie C (2019) Supersweet and waxy: meeting the diverse demands for specialty maize by genome editing. Plant Biotechnology Journal 17, 1853–1855.
Supersweet and waxy: meeting the diverse demands for specialty maize by genome editing.Crossref | GoogleScholarGoogle Scholar |

Du H, Liu H, Xiong L (2013a) Endogenous auxin and jasmonic acid levels are differentially modulated by abiotic stresses in rice. Frontiers in Plant Science 4, 397
Endogenous auxin and jasmonic acid levels are differentially modulated by abiotic stresses in rice.Crossref | GoogleScholarGoogle Scholar |

Du H, Wu N, Chang Y, Li X, Xiao J, Xiong L (2013b) Carotenoid deficiency impairs ABA and IAA biosynthesis and differentially affects drought and cold tolerance in rice. Plant Molecular Biology 83, 475–488.
Carotenoid deficiency impairs ABA and IAA biosynthesis and differentially affects drought and cold tolerance in rice.Crossref | GoogleScholarGoogle Scholar |

Gao Z, Feng H, Liang X, Zhang L, Lin S, Zhao X, Shen S, Zhou L, Zhou S (2018) Limits to maize productivity in the North China Plain: a comparison analysis for spring and summer maize. Field Crops Research 228, 39–47.
Limits to maize productivity in the North China Plain: a comparison analysis for spring and summer maize.Crossref | GoogleScholarGoogle Scholar |

Greaves JA (1996) Improving suboptimal temperature tolerance in maize- the search for variation. Journal of Experimental Botany 47, 307–323.
Improving suboptimal temperature tolerance in maize- the search for variation.Crossref | GoogleScholarGoogle Scholar |

Hetherington SE, Öquist G (1988) Monitoring chilling injury: a comparison of chlorophyll fluorescence measurements, post-chilling growth and visible symptoms of injury in Zea mays. Physiologia Plantarum 72, 241–247.
Monitoring chilling injury: a comparison of chlorophyll fluorescence measurements, post-chilling growth and visible symptoms of injury in Zea mays.Crossref | GoogleScholarGoogle Scholar |

Hu Y, Jiang Y, Han X, Wang H, Pan J, Yu D (2017) Jasmonate regulates leaf senescence and tolerance to cold stress: crosstalk with other phytohormones. Journal of Experimental Botany 68, 1361–1369.
Jasmonate regulates leaf senescence and tolerance to cold stress: crosstalk with other phytohormones.Crossref | GoogleScholarGoogle Scholar |

Huang M, Cao J, Liu Y, Zhang M, Hu L, Xiao Z, Chen J, Cao F (2021) Low-temperature stress during the flowering period alters the source–sink relationship and grain quality in field-grown late-season rice. Journal of Agronomy and Crop Science 207, 833–839.
Low-temperature stress during the flowering period alters the source–sink relationship and grain quality in field-grown late-season rice.Crossref | GoogleScholarGoogle Scholar |

Hüner NP, Bode R, Dahal K, Hollis L, Rosso D, Krol M, Ivanov AG (2012) Chloroplast redox imbalance governs phenotypic plasticity: the “grand design of photosynthesis” revisited. Frontiers in Plant Science 3, 255
Chloroplast redox imbalance governs phenotypic plasticity: the “grand design of photosynthesis” revisited.Crossref | GoogleScholarGoogle Scholar |

Ji H, Xiao L, Xia Y, Song H, Liu B, Tang L, Cao W, Zhu Y, Liu L (2017) Effects of jointing and booting low temperature stresses on grain yield and yield components in wheat. Agricultural and Forest Meteorology 243, 33–42.
Effects of jointing and booting low temperature stresses on grain yield and yield components in wheat.Crossref | GoogleScholarGoogle Scholar |

Kabir MH, Liu Q, Peng Q, Huang Z, Hong B, Li H, Xiao L (2014) Effect of temperature on chalkiness and related physiological and biochemical characteristics of early indica rice during grain filling. Research on Crops 15, 313–323.
Effect of temperature on chalkiness and related physiological and biochemical characteristics of early indica rice during grain filling.Crossref | GoogleScholarGoogle Scholar |

Kodra E, Steinhaeuser K, Ganguly AR (2011) Persisting cold extremes under 21st-century warming scenarios. Geophysical Research Letters 38, L08705
Persisting cold extremes under 21st-century warming scenarios.Crossref | GoogleScholarGoogle Scholar |

Li X, Cai J, Liu F, Dai T, Cao W, Jiang D (2014) Cold priming drives the sub-cellular antioxidant systems to protect photosynthetic electron transport against subsequent low temperature stress in winter wheat. Plant Physiology and Biochemistry 82, 34–43.
Cold priming drives the sub-cellular antioxidant systems to protect photosynthetic electron transport against subsequent low temperature stress in winter wheat.Crossref | GoogleScholarGoogle Scholar |

Liu M-Z, Osborne CP (2008) Leaf cold acclimation and freezing injury in C3 and C4 grasses of the Mongolian Plateau. Journal of Experimental Botany 59, 4161–4170.
Leaf cold acclimation and freezing injury in C3 and C4 grasses of the Mongolian Plateau.Crossref | GoogleScholarGoogle Scholar |

Liu L, Ji H, An J, Shi K, Ma J, Liu B, Tang L, Cao W, Zhu Y (2019) Response of biomass accumulation in wheat to low-temperature stress at jointing and booting stages. Environmental and Experimental Botany 157, 46–57.
Response of biomass accumulation in wheat to low-temperature stress at jointing and booting stages.Crossref | GoogleScholarGoogle Scholar |

Luo M, Shi Y, Yang Y, Zhao Y, Zhang Y, Shi Y, Kong M, Li C, Feng Z, Fan Y, Xu L, Xi S, Lu B, Zhao J (2020) Sequence polymorphism of the waxy gene in waxy maize accessions and characterization of a new waxy allele. Scientific Reports 10, 15851
Sequence polymorphism of the waxy gene in waxy maize accessions and characterization of a new waxy allele.Crossref | GoogleScholarGoogle Scholar |

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 |

Moradtalab N, Ahmed A, Geistlinger J, Walker F, Höglinger B, Ludewig U, Neumann G (2020) Synergisms of microbial consortia, N forms, and micronutrients alleviate oxidative damage and stimulate hormonal cold stress adaptations in maize. Frontiers in Plant Science 11, 396
Synergisms of microbial consortia, N forms, and micronutrients alleviate oxidative damage and stimulate hormonal cold stress adaptations in maize.Crossref | GoogleScholarGoogle Scholar |

Ortiz D, Hu J, Salas Fernandez MG (2017) Genetic architecture of photosynthesis in Sorghum bicolor under non-stress and cold stress conditions. Journal of Experimental Botany 68, 4545–4557.
Genetic architecture of photosynthesis in Sorghum bicolor under non-stress and cold stress conditions.Crossref | GoogleScholarGoogle Scholar |

Pamplona R (2011) Advanced lipoxidation end-products. Chemico-Biological Interactions 192, 14–20.
Advanced lipoxidation end-products.Crossref | GoogleScholarGoogle Scholar |

Peng X, Teng L, Yan X, Zhao M, Shen S (2015) The cold responsive mechanism of the paper mulberry: decreased photosynthesis capacity and increased starch accumulation. BMC Genomics 16, 898
The cold responsive mechanism of the paper mulberry: decreased photosynthesis capacity and increased starch accumulation.Crossref | GoogleScholarGoogle Scholar |

Pu L, Zhang S, Yang J, Chang L, Bai S (2019) Spatio-temporal dynamics of maize potential yield and yield gaps in Northeast China from 1990 to 2015. International Journal of Environmental Research and Public Health 16, 1211
Spatio-temporal dynamics of maize potential yield and yield gaps in Northeast China from 1990 to 2015.Crossref | GoogleScholarGoogle Scholar |

Ruban AV, Wentworth M, Yakushevska AE, Andersson J, Lee PJ, Keegstra W, Dekker JP, Boekema EJ, Jansson S, Horton P (2003) Plants lacking the main light-harvesting complex retain photosystem II macro-organization. Nature 421, 648–652.
Plants lacking the main light-harvesting complex retain photosystem II macro-organization.Crossref | GoogleScholarGoogle Scholar |

Shah K, Amin NU, Ahmad I, Ara G, Rahman MU, Zuo X, Xing L, Ren X (2019) Cement dust induce stress and attenuates photosynthesis in Arachis hypogaea. Environmental Science and Pollution Research 26, 19490–19501.
Cement dust induce stress and attenuates photosynthesis in Arachis hypogaea.Crossref | GoogleScholarGoogle Scholar |

Shibasaki K, Uemura M, Tsurumi S, Rahman A (2009) Auxin response in Arabidopsis under cold stress: underlying molecular mechanisms. The Plant Cell 21, 3823–3838.
Auxin response in Arabidopsis under cold stress: underlying molecular mechanisms.Crossref | GoogleScholarGoogle Scholar |

Siddik MA, Zhang J, Chen J, Qian H, Jiang Y, Raheem AK, Deng A, Song Z, Zheng C, Zhang W (2019) Responses of indica rice yield and quality to extreme high and low temperatures during the reproductive period. European Journal of Agronomy 106, 30–38.
Responses of indica rice yield and quality to extreme high and low temperatures during the reproductive period.Crossref | GoogleScholarGoogle Scholar |

Snider JL, Pilon C, Hu W, Wang H-M, Tishchenko V, Slaton W, Chastain D, Parkash V (2022) Net photosynthesis acclimates to low growth temperature in cotton seedlings by shifting temperature thresholds for photosynthetic component processes and respiration. Environmental and Experimental Botany 196, 104816
Net photosynthesis acclimates to low growth temperature in cotton seedlings by shifting temperature thresholds for photosynthetic component processes and respiration.Crossref | GoogleScholarGoogle Scholar |

Thakur P, Kumar S, Malik JA, Berger JD, Nayyar H (2010) Cold stress effects on reproductive development in grain crops: an overview. Environmental and Experimental Botany 67, 429–443.
Cold stress effects on reproductive development in grain crops: an overview.Crossref | GoogleScholarGoogle Scholar |

Tian B, Zhu J, Nie Y, Xu C, Meng Q, Wang P (2019) Mitigating heat and chilling stress by adjusting the sowing date of maize in the North China Plain. Journal of Agronomy and Crop Science 205, 77–87.
Mitigating heat and chilling stress by adjusting the sowing date of maize in the North China Plain.Crossref | GoogleScholarGoogle Scholar |

Tripathy BC, Oelmüller R (2012) Reactive oxygen species generation and signaling in plants. Plant Signaling & Behavior 7, 1621–1633.
Reactive oxygen species generation and signaling in plants.Crossref | GoogleScholarGoogle Scholar |

Valluru R, Link J, Claupein W (2012) Consequences of early chilling stress in two Triticum species: plastic responses and adaptive significance. Plant Biology 14, 641–651.
Consequences of early chilling stress in two Triticum species: plastic responses and adaptive significance.Crossref | GoogleScholarGoogle Scholar |

Venzhik Y, Talanova V, Titov A (2016) The effect of abscisic acid on cold tolerance and chloroplasts ultrastructure in wheat under optimal and cold stress conditions. Acta Physiologiae Plantarum 38, 63
The effect of abscisic acid on cold tolerance and chloroplasts ultrastructure in wheat under optimal and cold stress conditions.Crossref | GoogleScholarGoogle Scholar |

Wang S, Zhao H, Xiao C, Zhao L, Gu C, Na Y, Xie B, Cheng S (2016) Effects of cold stress during booting stage on dry matter production of rice in cold region. Chinese Journal of Rice Science 30, 313–322.
Effects of cold stress during booting stage on dry matter production of rice in cold region.Crossref | GoogleScholarGoogle Scholar |

Wang W, Wang X, Huang M, Cai J, Zhou Q, Dai T, Jiang D (2021) Alleviation of field low-temperature stress in winter wheat by exogenous application of salicylic acid. Journal of Plant Growth Regulation 40, 811–823.
Alleviation of field low-temperature stress in winter wheat by exogenous application of salicylic acid.Crossref | GoogleScholarGoogle Scholar |

Xu G, Singh SK, Reddy VR, Barnaby JY, Sicher RC, Li T (2016) Soybean grown under elevated CO2 benefits more under low temperature than high temperature stress: varying response of photosynthetic limitations, leaf metabolites, growth, and seed yield. Journal of Plant Physiology 205, 20–32.
Soybean grown under elevated CO2 benefits more under low temperature than high temperature stress: varying response of photosynthetic limitations, leaf metabolites, growth, and seed yield.Crossref | GoogleScholarGoogle Scholar |

Yamburenko MV, Zubo YO, Vanková R, Kusnetsov VV, Kulaeva ON, Börner T (2013) Abscisic acid represses the transcription of chloroplast genes. Journal of Experimental Botany 64, 4491–4502.
Abscisic acid represses the transcription of chloroplast genes.Crossref | GoogleScholarGoogle Scholar |

Yang H, Gu X, Ding M, Lu W, Lu D (2020) Weakened carbon and nitrogen metabolisms under post-silking heat stress reduce the yield and dry matter accumulation in waxy maize. Journal of Integrative Agriculture 19, 78–88.
Weakened carbon and nitrogen metabolisms under post-silking heat stress reduce the yield and dry matter accumulation in waxy maize.Crossref | GoogleScholarGoogle Scholar |

Ye Y, Wen Z, Yang H, Lu W, Lu D (2020) Effects of post-silking water deficit on the leaf photosynthesis and senescence of waxy maize. Journal of Integrative Agriculture 19, 2216–2228.
Effects of post-silking water deficit on the leaf photosynthesis and senescence of waxy maize.Crossref | GoogleScholarGoogle Scholar |

Ying J, Lee EA, Tollenaar M (2000) Response of maize leaf photosynthesis to low temperature during the grain-filling period. Field Crops Research 68, 87–96.
Response of maize leaf photosynthesis to low temperature during the grain-filling period.Crossref | GoogleScholarGoogle Scholar |

Ying J, Lee EA, Tollenaar M (2002) Response of leaf photosynthesis during the grain-filling period of maize to duration of cold exposure, acclimation, and incident PPFD. Crop Science 42, 1164–1172.
Response of leaf photosynthesis during the grain-filling period of maize to duration of cold exposure, acclimation, and incident PPFD.Crossref | GoogleScholarGoogle Scholar |

Yu J, Cang J, Lu Q, Fan B, Xu Q, Li W, Wang X (2020) ABA enhanced cold tolerance of wheat ‘dn1’ via increasing ROS scavenging system. Plant Signaling & Behavior 15, 1780403
ABA enhanced cold tolerance of wheat ‘dn1’ via increasing ROS scavenging system.Crossref | GoogleScholarGoogle Scholar |

Yu T, Zhang J, Cao J, Cai Q, Li X, Sun Y, Li S, Li Y, Hu G, Cao S, Liu C, Wang G, Wang L, Duan Y (2021) Leaf transcriptomic response mediated by cold stress in two maize inbred lines with contrasting tolerance levels. Genomics 113, 782–794.
Leaf transcriptomic response mediated by cold stress in two maize inbred lines with contrasting tolerance levels.Crossref | GoogleScholarGoogle Scholar |

Zhang W, Wang J, Huang Z, Mi L, Xu K, Wu J, Fan Y, Ma S, Jiang D (2019) Effects of low temperature at booting stage on sucrose metabolism and endogenous hormone contents in winter wheat spikelet. Frontiers in Plant Science 10, 498
Effects of low temperature at booting stage on sucrose metabolism and endogenous hormone contents in winter wheat spikelet.Crossref | GoogleScholarGoogle Scholar |

Zhang W, Zhao Y, Li L, Yang L, Luo Z, Wang B, Ma S, Fan Y, Huang Z (2021) The effects of short-term exposure to low temperatures during the booting stage on starch synthesis and yields in wheat grain. Frontiers in Plant Science 12, 684784
The effects of short-term exposure to low temperatures during the booting stage on starch synthesis and yields in wheat grain.Crossref | GoogleScholarGoogle Scholar |

Zhao Y, Han Q, Ding C, Huang Y, Liao J, Chen T, Feng S, Zhou L, Zhang Z, Chen Y, Yuan S, Yuan M (2020) Effect of low temperature on chlorophyll biosynthesis and chloroplast biogenesis of rice seedlings during greening. International Journal of Molecular Sciences 21, 1390
Effect of low temperature on chlorophyll biosynthesis and chloroplast biogenesis of rice seedlings during greening.Crossref | GoogleScholarGoogle Scholar |

Zhao B, Liu Q, Wang B, Yuan F (2021) Roles of phytohormones and their signaling pathways in leaf development and stress responses. Journal of Agricultural and Food Chemistry 69, 3566–3584.
Roles of phytohormones and their signaling pathways in leaf development and stress responses.Crossref | GoogleScholarGoogle Scholar |

Zhou R, Yu X, Zhao T, Ottosen CO, Rosenqvist E, Wu Z (2019) Physiological analysis and transcriptome sequencing reveal the effects of combined cold and drought on tomato leaf. BMC Plant Biology 19, 377
Physiological analysis and transcriptome sequencing reveal the effects of combined cold and drought on tomato leaf.Crossref | GoogleScholarGoogle Scholar |

Žydelis R, Weihermüller L, Herbst M, Klosterhalfen A, Lazauskas S (2018) A model study on the effect of water and cold stress on maize development under nemoral climate. Agricultural and Forest Meteorology 263, 169–179.
A model study on the effect of water and cold stress on maize development under nemoral climate.Crossref | GoogleScholarGoogle Scholar |