Phenotypic, Physiological and Hormonal Analysis Reveals the Mechanisms of Timely Harvesting for Ensuring the Seed Vigor of Maize (Zea mays L.) Inbred Lines
Abstract
:1. Introduction
2. Materials and Methods
2.1. Material Planting and Collection
2.2. Phenotypic Analysis and Moisture Content Detemination
2.3. Germination Assay
2.4. Determination of Soluble Sugar Content
2.5. Determination of Antioxidant Enzyme Activities
2.6. Determination of the Endogenous Hormone Content
2.7. Statistical Analysis
3. Results
3.1. Phenotypic and Moisture Characteristic Changes in Seeds and Embryos at Different Harvest Stages
3.2. Changes of Seed Vigor in Maize Inbred Lines at Different Harvest Stages
3.3. Physiological Trait Changes in Fresh Seed Embryos at Different Harvest Stages
3.3.1. Soluble Sugar Content
3.3.2. Antioxidant Enzyme Activity
3.3.3. Hormone Levels
3.4. Correlation among the Seed Vigor Indexes and Phenotypic and Physiological Traits
4. Discussion
4.1. Timely Harvest Is a Prerequisite for Ensuring the Seed Vigor of Maize Inbred Lines
4.2. The Soluble Sugar Content of Fresh Embryos Is Not the Key Factor for Maintaining Seed Vigor after Drying
4.3. Antioxidant Enzymes in Developing Embryos Play Important Roles in Ensuring Seed Vigor after Drying
4.4. Pythormones Participate in Establishing Embryo Morphogenesis to Improve Seed Vigor
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Data Availability Statement
Conflicts of Interest
References
- Riedelsheimer, C.; Czedik-Eysenberg, A.; Grieder, C.; Lisec, J.; Technow, F.; Sulpice, R.; Altmann, T.; Stitt, M.; Willmitzer, L.; Melchinger, A.E. Genomic and metabolic prediction of complex heterotic traits in hybrid maize. Nat. Genet. 2012, 44, 217–220. [Google Scholar] [CrossRef] [PubMed]
- Venkatesh, T.V.; Breeze, M.L.; Liu, K.; Harrigan, G.G.; Culler, A.H. Compositional analysis of grain and forage from MON 87427, an inducible male sterile and tissue selective glyphosate-tolerant maize product for hybrid seed production. J. Agric. Food Chem. 2014, 62, 1964–1973. [Google Scholar] [CrossRef]
- García-Lara, S.; Serna-Saldivar, S.O. Chapter 1—Corn History and Culture. In Corn, 3rd ed.; Serna-Saldivar, S.O., Ed.; AACC International Press: Oxford, UK, 2019; pp. 1–18. [Google Scholar]
- Mondo, V.H.V.; Cicero, S.M.; Dourado-Neto, D.; Pupim, T.L.; Dias, M.A.N. Effect of Seed Vigor on Intraspecific Competition and Grain Yield in Maize. Agron. J. 2013, 105, 222–228. [Google Scholar] [CrossRef]
- Zhao, L.; Han, Z.; Yang, J.; Qi, H. Single seed precise sowing of maize using computer simulation. PLoS ONE 2018, 13, e0193750. [Google Scholar] [CrossRef]
- Marcos-Filho, J. Seed vigor testing: An overview of the past, present and future perspective. Sci. Agric. 2015, 72, 363–374. [Google Scholar] [CrossRef]
- Zhang, Q.; Song, X.; Bartels, D. Enzymes and Metabolites in Carbohydrate Metabolism of Desiccation Tolerant Plants. Proteomes 2016, 4, 40. [Google Scholar] [CrossRef]
- Reed, R.C.; Bradford, K.J.; Khanday, I. Seed germination and vigor: Ensuring crop sustainability in a changing climate. Heredity 2022, 128, 450–459. [Google Scholar] [CrossRef]
- Omar, S.; Abd Ghani, R.; Khalid, N.; Jolánkai, M.; Tarnawa, Á.; Percze, A.; Mikó, P.P.; Kende, Z. Effects of Seed Quality and Hybrid Type on Maize Germination and Yield in Hungary. Agriculture 2023, 13, 1836. [Google Scholar] [CrossRef]
- Xing, M.; Long, Y.; Wang, Q.; Tian, X.; Fan, S.; Zhang, C.; Huang, W.J.A. Physiological alterations and nondestructive test methods of crop seed vigor: A comprehensive review. Agriculture 2023, 13, 527. [Google Scholar] [CrossRef]
- Finkelstein, R.R. The Role of Hormones during Seed Development and Germination. In Plant Hormones: Biosynthesis, Signal Transduction, Action! Davies, P.J., Ed.; Springer: Dordrecht, The Netherlands, 2010; pp. 549–573. [Google Scholar]
- Jin, X.; Liu, Z.; Wu, W. Corn harvesting time based on growth curve and antioxidant enzyme activity. Int. J. Food Prop. 2024, 27, 1–11. [Google Scholar] [CrossRef]
- Afzal, S.; Chaudhary, N.; Singh, N.K. Role of Soluble Sugars in Metabolism and Sensing Under Abiotic Stress. In Plant Growth Regulators: Signalling under Stress Conditions; Aftab, T., Hakeem, K.R., Eds.; Springer International Publishing: Cham, Switzerland, 2021; pp. 305–334. [Google Scholar]
- Samarah, N.H.; Mullen, R.E.; Anderson, I. Soluble Sugar Contents, Germination, and Vigor of Soybean Seeds in Response to Drought Stress. J. New Seeds 2009, 10, 63–73. [Google Scholar] [CrossRef]
- Wulansari, R.; Farhana, B.; Fajrina, N. Field Emergence Test in Relation to Laboratory Seed Quality Tests of Sweet Corn Seed. IOP Conf. Ser. Earth Environ. Sci. 2023, 1160, 012017. [Google Scholar] [CrossRef]
- Vaistij, F.E.; Gan, Y.; Penfield, S.; Gilday, A.D.; Dave, A.; He, Z.; Josse, E.-M.; Choi, G.; Halliday, K.J.; Graham, I.A. Differential control of seed primary dormancy in Arabidopsis ecotypes by the transcription factor SPATULA. Proc. Natl. Acad. Sci. USA 2013, 110, 10866–10871. [Google Scholar] [CrossRef] [PubMed]
- Kermode, A.R. Role of Abscisic Acid in Seed Dormancy. J. Plant Growth Regul. 2005, 24, 319–344. [Google Scholar] [CrossRef]
- Nambara, E.; Okamoto, M.; Tatematsu, K.; Yano, R.; Seo, M.; Kamiya, Y. Abscisic acid and the control of seed dormancy and germination. Seed Sci. Res. 2010, 20, 55–67. [Google Scholar] [CrossRef]
- Hilhorst, H.W.M.; Karssen, C.M. Seed dormancy and germination: The role of abscisic acid and gibberellins and the importance of hormone mutants. Plant Growth Regul. 1992, 11, 225–238. [Google Scholar] [CrossRef]
- Yamaguchi, S.; Smith, M.W.; Brown, R.G.S.; Kamiya, Y.; Sun, T.-P. Phytochrome Regulation and Differential Expression of Gibberellin 3β-Hydroxylase Genes in Germinating Arabidopsis Seeds. Plant Cell 1998, 10, 2115–2126. [Google Scholar] [CrossRef] [PubMed]
- Tuan, P.A.; Kumar, R.; Rehal, P.K.; Toora, P.K.; Ayele, B.T. Molecular Mechanisms Underlying Abscisic Acid/Gibberellin Balance in the Control of Seed Dormancy and Germination in Cereals. Front. Plant Sci. 2018, 9, 668. [Google Scholar] [CrossRef] [PubMed]
- Wang, Y.; Li, L.; Ye, T.; Zhao, S.; Liu, Z.; Feng, Y.-Q.; Wu, Y. Cytokinin antagonizes ABA suppression to seed germination of Arabidopsis by downregulating ABI5 expression. Plant J. 2011, 68, 249–261. [Google Scholar] [CrossRef]
- Khan, A.A. Inhibition of Gibberellic Acid-induced Germination by Abscisic Acid and Reversal by Cytokinins 12. Plant Physiol. 1968, 43, 1463–1465. [Google Scholar] [CrossRef]
- Eastwood, D.; Tavener, R.J.A.; Laidman, D.L. Sequential Action of Cytokinin and Gibberellic Acid in Wheat Aleurone Tissue. Nature 1969, 221, 1267. [Google Scholar] [CrossRef] [PubMed]
- Farooq, M.A.; Ma, W.; Shen, S.; Gu, A. Underlying Biochemical and Molecular Mechanisms for Seed Germination. Int. J. Mol. Sci. 2022, 23, 8502. [Google Scholar] [CrossRef] [PubMed]
- Fu, Y.; Ma, L.; Li, J.; Hou, D.; Zeng, B.; Zhang, L.; Liu, C.; Bi, Q.; Tan, J.; Yu, X.; et al. Factors Influencing Seed Dormancy and Germination and Advances in Seed Priming Technology. Plants 2024, 13, 1319. [Google Scholar] [CrossRef]
- Guangwu, Z.; Xuwen, J. Roles of Gibberellin and Auxin in Promoting Seed Germination and Seedling Vigor in Pinus massoniana. For. Sci. 2014, 60, 367–373. [Google Scholar] [CrossRef]
- Matilla, A.J. Auxin: Hormonal Signal Required for Seed Development and Dormancy. Plants 2020, 9, 705. [Google Scholar] [CrossRef] [PubMed]
- Gu, R.; Li, L.; Liang, X.; Wang, Y.; Fan, T.; Wang, Y.; Wang, J. The ideal harvest time for seeds of hybrid maize (Zea mays L.) XY335 and ZD958 produced in multiple environments. Sci. Rep. 2017, 7, 17537. [Google Scholar] [CrossRef]
- Li, H.; Yue, H.; Li, L.; Su, C.; Zhang, X.; Liu, J.; Yu, Z.; Zhao, G.; Song, X.; Wang, J.; et al. A Comparative Analysis of the Hybrid Maize (Zea mays L.) Seed Quality in China from 2013 to 2018. Agronomy 2019, 9, 625. [Google Scholar] [CrossRef]
- Shi, Y.; Li, G.; Tian, Z.; Wang, Z.; Wang, X.; Zhu, Y.; Chen, Y.; Guo, S.; Qi, J.; Zhang, X.I.N.; et al. Genetic dissection of seed vigour traits in maize (Zea mays L.) under low-temperature conditions. J. Genet. 2016, 95, 1017–1022. [Google Scholar] [CrossRef]
- Han, D.; Hu, H.; Yang, J.; Liang, X.; Ai, J.; Abula, A.; Li, M.; Wang, Y.; Xi, H.; Li, L.; et al. The ideal harvest time for seed production in maize (Zea mays L.) varieties of different maturity groups. J. Sci. Food Agric. 2022, 102, 5867–5874. [Google Scholar] [CrossRef]
- Lee, M. Inbred Lines of Maize and Their Molecular Markers. In The Maize Handbook; Freeling, M., Walbot, V., Eds.; Springer: New York, NY, USA, 1994; pp. 423–432. [Google Scholar]
- Wang, M.; Qu, H.; Zhang, H.; Liu, S.; Li, Y.; Zhang, C. Hormone and RNA-seq analyses reveal the mechanisms underlying differences in seed vigour at different maize ear positions. Plant Mol. Biol. 2019, 99, 461–476. [Google Scholar] [CrossRef]
- Li, Y.; Qu, H.; Zhu, P.; Su, K.; Zhang, C. Comparative Proteomics Reveals the Mechanisms Underlying Variations in Seed Vigor Based on Maize (Zea mays L.) Ear Positions. Plant Mol. Biol. Report. 2018, 36, 738–749. [Google Scholar] [CrossRef]
- Hay, F.; Rezaei, S.; Wolkis, D.; McGill, C. Determination and Control of Seed Moisture. Seed Sci. Technol. 2023, 51, 267–285. [Google Scholar] [CrossRef]
- Windham, G.L.; Williams, W.P.; Mylroie, J.E.; Reid, C.X.; Womack, E.D. A Histological Study of Aspergillus flavus Colonization of Wound Inoculated Maize Kernels of Resistant and Susceptible Maize Hybrids in the Field. Front. Microbiol. 2018, 9, 799. [Google Scholar] [CrossRef] [PubMed]
- Wood, I.P.; Elliston, A.; Ryden, P.; Bancroft, I.; Roberts, I.N.; Waldron, K.W. Rapid quantification of reducing sugars in biomass hydrolysates: Improving the speed and precision of the dinitrosalicylic acid assay. Biomass Bioenergy 2012, 44, 117–121. [Google Scholar] [CrossRef]
- Miller, G.L. Use of Dinitrosalicylic Acid Reagent for Determination of Reducing Sugar. Anal. Chem. 1959, 31, 426–428. [Google Scholar] [CrossRef]
- Yang, X.; Gan, L.; Ruan, H. Influence of nitrogen on the activities of POD and SOD in rice seedlings and the incidence of rice blast disease. J. Fujian Agric. For. Univ. Nat. Sci. Ed. 2011, 40, 8–12. [Google Scholar]
- Bailly, C.; Benamar, A.; Corbineau, F.; Come, D. Changes in malondialdehyde content and in superoxide dismutase, catalase and glutathione reductase activities in sunflower seeds as related to deterioration during accelerated aging. Physiol. Plant. 1996, 97, 104–110. [Google Scholar] [CrossRef]
- Scebba, F.; Sebastiani, L.; Vitagliano, C. Activities of Antioxidant Enzymes during Senescence of Prunus armeniaca Leaves. Biol. Plant. 2001, 44, 41–46. [Google Scholar] [CrossRef]
- Doddagoudar, S.R.; Nagaraja, M.; Lakshmikanth, M.; Srininvas, A.G.; Shakuntala, N.M.; Umesh, H.; Mahanthshivayogayya, K. Improving the resilience of rice seedlings to low temperature stress through seed priming. South Afr. J. Bot. 2023, 162, 183–192. [Google Scholar]
- Zhang, C.; Bruins, M.E.; Yang, Z.; Liu, S.; Rao, P. A new formula to calculate activity of superoxide dismutase in indirect assays. Anal. Biochem. 2016, 503, 65–67. [Google Scholar] [CrossRef]
- Tierney, L. The R Statistical Computing Environment. In Statistical Challenges in Modern Astronomy V; Springer: New York, NY, USA, 2012; pp. 435–447. [Google Scholar]
- Shi, R.; Tong, L.; Du, T.; Shukla, M.K. Response and Modeling of Hybrid Maize Seed Vigor to Water Deficit at Different Growth Stages. Water 2020, 12, 3289. [Google Scholar] [CrossRef]
- Chaengsakul, C.; Onwimol, D.; Kongsil, P.; Suwannarat, S. Ethanol production and mitochondrial-related gene expression of maize (Zea mays) seed during storage. J. Integr. Agric. 2019, 18, 2435–2445. [Google Scholar] [CrossRef]
- Fu, H.; Cao, D.-D.; Hu, W.-M.; Guan, Y.-J.; Fu, Y.-Y.; Fang, Y.-F.; Hu, J. Studies on optimum harvest time for hybrid rice seed. J. Sci. Food Agric. 2017, 97, 1124–1133. [Google Scholar] [CrossRef]
- Jiang, L.; Wang, M.; Chu, Z.; Gao, Y.; Guo, L.; Ji, S.; Jiang, L.; Gong, L. Effects of Temperature on Growth and Grain Maturity of Spring Maize in Northeast China: A Study of Different Sowing Dates. Atmosphere 2023, 14, 1755. [Google Scholar] [CrossRef]
- Li, W.; Yu, Y.; Wang, L.; Luo, Y.; Peng, Y.; Xu, Y.; Liu, X.; Wu, S.; Jian, L.; Xu, J.; et al. The genetic architecture of the dynamic changes in grain moisture in maize. Plant Biotechnol. J. 2021, 19, 1195–1205. [Google Scholar] [CrossRef] [PubMed]
- Bewleyjd, B.M. Physiology and biochemistry of seeds in relation to germination. Vegetatio 1984, 57, 115–119. [Google Scholar]
- Poonam Bhardwaj, R.; Handa, N.; Kaur, H.; Rattan, A.; Bali, S.; Gautam, V.; Sharma, A.; Ohri, P.; Thukral, A.K. Sugar signalling in plants. In Water Stress and Crop Plants: A Sustainable Approach; Wiley: Hoboken, NJ, USA, 2016; pp. 287–302. [Google Scholar]
- Nishizawa, A.; Yabuta, Y.; Shigeoka, S. Galactinol and Raffinose Constitute a Novel Function to Protect Plants from Oxidative Damage. Plant Physiol. 2008, 147, 1251–1263. [Google Scholar] [CrossRef]
- Shen, S.; Ma, S.; Chen, X.-M.; Yi, F.; Li, B.-B.; Liang, X.-G.; Liao, S.-J.; Gao, L.-H.; Zhou, S.-L.; Ruan, Y.-L. A transcriptional landscape underlying sugar import for grain set in maize. Plant J. 2022, 110, 228–242. [Google Scholar] [CrossRef]
- Berjak, P.; Farrant, J.M.; Pammenter, N.W. Seed Desiccation-Tolerance Mechanisms. In Plant Desiccation Tolerance; Wiley: Hoboken, NJ, USA, 2007; pp. 149–192. [Google Scholar]
- Adetunji, A.E.; Adetunji, T.L.; Varghese, B.; Sershen Pammenter, N.W. Oxidative Stress, Ageing and Methods of Seed Invigoration: An Overview and Perspectives. Agronomy 2021, 11, 2369. [Google Scholar] [CrossRef]
- Li, W.; Niu, Y.; Zheng, Y.; Wang, Z. Advances in the Understanding of Reactive Oxygen Species-Dependent Regulation on Seed Dormancy, Germination, and Deterioration in Crops. Front. Plant Sci. 2022, 13, 826809. [Google Scholar] [CrossRef]
- Bailly, C.; El-Maarouf-Bouteau, H.; Corbineau, F. From intracellular signaling networks to cell death: The dual role of reactive oxygen species in seed physiology. Comptes Rendus Biol. 2008, 331, 806–814. [Google Scholar] [CrossRef] [PubMed]
- Sveinsdóttir, H.; Yan, F.; Zhu, Y.; Peiter-Volk, T.; Schubert, S. Seed ageing-induced inhibition of germination and post-germination root growth is related to lower activity of plasma membrane H+-ATPase in maize roots. J. Plant Physiol. 2009, 166, 128–135. [Google Scholar] [CrossRef]
- Li, Z.; Zhang, J.; Liu, Y.; Zhao, J.; Fu, J.; Ren, X.; Wang, G.; Wang, J. Exogenous auxin regulates multi-metabolic network and embryo development, controlling seed secondary dormancy and germination in Nicotiana tabacum L. BMC Plant Biol. 2016, 16, 41. [Google Scholar] [CrossRef]
- Locascio, A.; Roig-Villanova, I.; Bernardi, J.; Varotto, S. Current perspectives on the hormonal control of seed development in Arabidopsis and maize: A focus on auxin. Front. Plant Sci. 2014, 5, 412. [Google Scholar] [CrossRef] [PubMed]
- Thomas, S.G.; Rieu, I.; Steber, C.M. Gibberellin metabolism and signaling. Vitam. Horm. 2005, 72, 289–338. [Google Scholar] [PubMed]
- Urbanova, T.; Leubner-Metzger, G. Gibberellins and seed germination. Annu. Plant Rev. 2016, 49, 253–284. [Google Scholar]
- Ali, F.; Qanmber, G.; Li, F.; Wang, Z. Updated role of ABA in seed maturation, dormancy, and germination. J. Adv. Res. 2022, 35, 199–214. [Google Scholar] [CrossRef] [PubMed]
- Kozaki, A.; Aoyanagi, T. Molecular Aspects of Seed Development Controlled by Gibberellins and Abscisic Acids. Int. J. Mol. Sci. 2022, 23, 1876. [Google Scholar] [CrossRef]
- Figueiredo, D.D.; Köhler, C. Auxin: A molecular trigger of seed development. Genes Dev. 2018, 32, 479–490. [Google Scholar] [CrossRef] [PubMed]
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Feng, W.; Wang, H.; Bai, Y.; Wang, W.; Xue, W.; Shi, Z.; Qiu, P.; Gao, Y.; Xue, J.; Sun, M.; et al. Phenotypic, Physiological and Hormonal Analysis Reveals the Mechanisms of Timely Harvesting for Ensuring the Seed Vigor of Maize (Zea mays L.) Inbred Lines. Agronomy 2024, 14, 1770. https://doi.org/10.3390/agronomy14081770
Feng W, Wang H, Bai Y, Wang W, Xue W, Shi Z, Qiu P, Gao Y, Xue J, Sun M, et al. Phenotypic, Physiological and Hormonal Analysis Reveals the Mechanisms of Timely Harvesting for Ensuring the Seed Vigor of Maize (Zea mays L.) Inbred Lines. Agronomy. 2024; 14(8):1770. https://doi.org/10.3390/agronomy14081770
Chicago/Turabian StyleFeng, Wanjun, Haoxue Wang, Yu Bai, Weijie Wang, Weiwei Xue, Zhaokang Shi, Peng Qiu, Yu Gao, Jianfu Xue, Min Sun, and et al. 2024. "Phenotypic, Physiological and Hormonal Analysis Reveals the Mechanisms of Timely Harvesting for Ensuring the Seed Vigor of Maize (Zea mays L.) Inbred Lines" Agronomy 14, no. 8: 1770. https://doi.org/10.3390/agronomy14081770