Advertisement

Hormone and RNA-seq analyses reveal the mechanisms underlying differences in seed vigour at different maize ear positions

  • Mingming Wang
  • Haibin Qu
  • Huidi Zhang
  • Shuai Liu
  • Yan LiEmail author
  • Chunqing ZhangEmail author
Article

Abstract

Key message

ABA/GA4 ratio, stress resistance, carbon and nitrogen metabolism, and chromatin structure play important roles in vigour differences of seeds located at different maize ear positions.

Abstract

Seed vigour, which ensures rapid and uniform field emergence across diverse environments, differs at different maize ear positions. However, little is known regarding the associated mechanisms. In this study, we determined that seed vigour, stress resistance, and carbon and nitrogen metabolism were higher in seeds from middle and bottom section of the ear, while the ABA/GA4 ratio in the embryos was significantly lower. Compared with the seeds subjected to repeated pollination during silking, less variation in seed vigour and the ABA/GA4 ratio in the embryos was observed in seeds at different ear positions subjected to single pollination after complete silking. This indicated that single pollination can reduce, but not eliminate, the differences in seed vigour at different ear positions. RNA-seq analysis indicated that the seed vigour differences at the different locations of the maize ears of the single pollinated treatment were related to carbon and nitrogen metabolism. In contrast, the differences in seed vigour under repeated pollination were related to chromatin structure. The present study contributes to our understanding of the mechanisms underlying differences in seed vigour at different positions on the maize ear.

Keywords

ABA GA4 Seed position Seed vigour Zea mays 

Notes

Acknowledgements

We thank Professor Gerhard Leubner-Metzger and Waheed Arshad, Royal Holloway, University of London, United Kingdom, for reading and providing valuable comments on this manuscript. This work was supported by the grants from the National Natural Science Foundation of China (Grant Nos. 31271808 and 31771890).

Author contributions

YL and CZ planned and designed the research. MW, HQ, HZ and SL conducted experiments. WM, YL and CZ analyzed the data. WM and YL wrote the paper.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

11103_2019_830_MOESM1_ESM.pdf (92 kb)
Supplementary material 1 (PDF 91 KB)
11103_2019_830_MOESM2_ESM.xlsx (13 kb)
Supplementary material 2 (XLSX 13 KB)
11103_2019_830_MOESM3_ESM.pdf (255 kb)
Supplementary material 3 (PDF 255 KB)
11103_2019_830_MOESM4_ESM.pdf (573 kb)
Supplementary material 4 (PDF 572 KB)
11103_2019_830_MOESM5_ESM.xlsx (25 kb)
Supplementary material 5 (XLSX 25 KB)

References

  1. Bai B, Sikron N, Gendler T, Kazachkova Y, Barak S, Grafi G, Khozin-Goldberg I, Fait A (2012) Ecotypic variability in the metabolic response of seeds to diurnal hydration-dehydration cycles and its relationship to seed vigor. Plant Cell Physiol 53:38–52CrossRefGoogle Scholar
  2. Bewley JD, Bradford KJ, Hilhorst HWM, Nonogaki H (2013) Seeds: physiology of development, germination and dormancy. Springer, New YorkCrossRefGoogle Scholar
  3. Boccaccini A, Lorrai R, Ruta V, Frey A, Mercey-Boutet S, Marion-Poll A, Tarkowská D, Strnad M, Costantino P, Vittorioso P (2016) The DAG1 transcription factor negatively regulates the seed-to-seedling transition in Arabidopsis acting on ABA and GA levels. BMC Plant Biol 16:198CrossRefGoogle Scholar
  4. Catusse J, Meinhard J, Job C, Strub JM, Fischer U, Pestsova E, Westhoff P, Van Dorsselaer A, Job D (2011) Proteomics reveals potential biomarkers of seed vigor in sugarbeet. Proteomics 11:1569–1580CrossRefGoogle Scholar
  5. Chang C, Wang B, Shi L, Li Y, Duo L, Zhang W (2010) Alleviation of salt stress-induced inhibition of seed germination in cucumber (Cucumis sativus L.) by ethylene and glutamate. J Plant Physiol 167:1152–1156CrossRefGoogle Scholar
  6. da Silva EA, Toorop PE, van Aelst AC, Hilhorst HW (2004) Abscisic acid controls embryo growth potential and endosperm cap weakening during coffee (Coffea arabica cv. Rubi) seed germination. Planta 220:251–261CrossRefGoogle Scholar
  7. Dave A, Hernandez ML, He Z, Andriotis VM, Vaistij FE, Larson TR, Graham IA (2011) 12-oxo-phytodienoic acid accumulation during seed development represses seed germination in Arabidopsis. Plant Cell 23:583–599CrossRefGoogle Scholar
  8. Deng ZJ, Hu XF, Ai XR, Yao L, Deng SM, Pu X, Song SQ (2015) Dormancy release of Cotinus coggygria seeds under a pre-cold moist stratification: an endogenous abscisic acid/gibberellic acid and comparative proteomic analysis. N For 47:105–118Google Scholar
  9. Finch-Savage WE, Bassel GW (2016) Seed vigour and crop establishment: extending performance beyond adaptation. J Exp Bot 67:567–591CrossRefGoogle Scholar
  10. Galleschi L, Capocchi A, Ghiringhelli S, Saviozzi F (2002) Antioxidants, free radicals, storage proteins, and proteolytic activities in wheat (Triticum durum) seeds during accelerated aging. J Agric Food Chem 50:5450–5457CrossRefGoogle Scholar
  11. Gallardo M, Rueda PMD, Matilla AJ, Sánchez-Calle IM (1994) Effect of short-chain fatty acids on the ethylene pathway in embryonic axes of cicer arietinum, during germination. Physiol Plant 92:629–635CrossRefGoogle Scholar
  12. Girhepuje PV, Shinde GB (2011) Transgenic tomato plants expressing a wheat endochitinase gene demonstrate enhanced resistance to Fusarium oxysporum f. sp. lycopersici. Plant Cell Tiss Org 105:243–251CrossRefGoogle Scholar
  13. Han Z, Ku L, Zhang Z, Zhang J, Guo S, Liu H, Zhao R, Ren Z, Zhang L, Su H, Dong L, Chen Y (2014) QTLs for seed vigor-related traits identified in maize seeds germinated under artificial aging conditions. PLoS ONE 9:e92535CrossRefGoogle Scholar
  14. Henikoff S, Smith MM (2015) Histone variants and epigenetics. CSH Perspect Biol 7:a019364Google Scholar
  15. Kirma M, Araujo WL, Fernie AR, Galili G (2012) The multifaceted role of aspartate-family amino acids in plant metabolism. J Exp Bot 63:4995–5001CrossRefGoogle Scholar
  16. Kucera B, Cohn MA, Leubner-Metzger G (2005) Plant hormone interactions during seed dormancy release and germination. Seed Sci Res 15:281–307CrossRefGoogle Scholar
  17. Lee YP, Baek K-H, Lee H-S, Kwak S-S, Bang J-W, Kwon S-Y (2010) Tobacco seeds simultaneously over-expressing Cu/Zn-superoxide dismutase and ascorbate peroxidase display enhanced seed longevity and germination rates under stress conditions. J Exp Bot 61:2499–2506CrossRefGoogle Scholar
  18. Li T, Zhang Y, Wang D, Liu Y, Dirk LMA, Goodman J, Downie AB, Wang J, Wang G, Zhao T (2017) Regulation of seed vigor by manipulation of raffinose family oligosaccharides (RFOs) in maize and arabidopsis. Mol Plant 10:1540–1555CrossRefGoogle Scholar
  19. Liu Y, Koornneef M, Soppe WJ (2007) The absence of histone H2B monoubiquitination in the Arabidopsis hub1 (rdo4) mutant reveals a role for chromatin remodeling in seed dormancy. Plant Cell 19:433–444CrossRefGoogle Scholar
  20. Liu Y, Fang J, Xu F, Chu J, Yan C, Schlappi MR, Wang Y, Chu C (2014) Expression patterns of ABA and GA metabolism genes and hormone levels during rice seed development and imbibition: a comparison of dormant and non-dormant rice cultivars. J Genet Genom 41:327–338CrossRefGoogle Scholar
  21. Marquez-Millano A, Elam WW, Blanche CA (1991) Influence of accelerated aging on fatty acid composition of slash pine (Pinus Elliottii engelm. var. Elliottii) seeds. J Seed Technol 15:29–41Google Scholar
  22. Mondo VH, Cicero SM (2005) Using image analysis to evaluate the quality of maize seeds located in different positions on the ear. Rev Bras Sementes 27:9–18CrossRefGoogle Scholar
  23. Nakabayashi K, Okamoto M, Koshiba T, Kamiya Y, Nambara E (2005) Genome-wide profiling of stored mRNA in Arabidopsis thaliana seed germination: epigenetic and genetic regulation of transcription in seed. Plant J 41:697–709CrossRefGoogle Scholar
  24. Nolan KE, Song Y, Liao S, Saeed NA, Zhang X, Rose RJ (2014) An unusual abscisic acid and gibberellic acid synergism increases somatic embryogenesis, facilitates its genetic analysis and improves transformation in Medicago truncatula. PLoS ONE 9:e99908CrossRefGoogle Scholar
  25. Ogawa M, Hanada A, Yamauchi Y, Kuwahara A, Kamiya Y, Yamaguchi S (2003) Gibberellin biosynthesis and response during Arabidopsis seed germination. Plant Cell 15:1591–1604CrossRefGoogle Scholar
  26. Okamoto M, Kuwahara A, Seo M, Kushiro T, Asami T, Hirai N, Kamiya Y, Koshiba T, Nambara E (2006) CYP707A1 and CYP707A2, which encode abscisic acid 8′-hydroxylases, are indispensable for proper control of seed dormancy and germination in Arabidopsis. Plant Physiol 141:97–107CrossRefGoogle Scholar
  27. Okamoto M, Tatematsu K, Matsui A, Morosawa T, Ishida J, Tanaka M, Endo TA, Mochizuki Y, Toyoda T, Kamiya Y, Shinozaki K, Nambara E, Seki M (2010) Genome-wide analysis of endogenous abscisic acid-mediated transcription in dry and imbibed seeds of Arabidopsis using tiling arrays. Plant J 62:39–51CrossRefGoogle Scholar
  28. Petla BP, Kamble NU, Kumar M, Verma P, Ghosh S, Singh A, Rao V, Salvi P, Kaur H, Saxena SC, Majee M (2016) Rice PROTEIN l-ISOASPARTYL METHYLTRANSFERASE isoforms differentially accumulate during seed maturation to restrict deleterious isoAsp and reactive oxygen species accumulation and are implicated in seed vigor and longevity. New Phytol 211:627–645CrossRefGoogle Scholar
  29. Rajeswari MR, Jain A (2002) High-mobility-group chromosomal proteins, HMGA1 as potential tumour markers. Curr Sci India 82:838–844Google Scholar
  30. Rajjou L, Gallardo K, Debeaujon I, Vandekerckhove J, Job C, Job D (2004) The effect of alpha-amanitin on the Arabidopsis seed proteome highlights the distinct roles of stored and neosynthesized mRNAs during germination. Plant Physiol 134:1598–1613CrossRefGoogle Scholar
  31. Rajjou L, Duval M, Gallardo K, Catusse J, Bally J, Job C, Job D (2012) Seed germination and vigor. Annu Rev Plant Biol 63:507–533CrossRefGoogle Scholar
  32. Revilla P, Butron A, Rodriguez VM, Malvar RA, Ordas A (2009) Identification of genes related to germination in aged maize seed by screening natural variability. J Exp Bot 60:4151–4157CrossRefGoogle Scholar
  33. Rock CD, Quatrano RS (1995) The role of hormones during seed development. In: Davies PJ (ed) Plant hormones. Springer, Dordrecht, pp 671–697CrossRefGoogle Scholar
  34. Shen S, Zhang L, Liang XG, Zhao X, Lin S, Qu LH, Liu YP, Gao Z, Ruan YL, Zhou SL (2018) Delayed pollination and low availability of assimilates are major factors causing maize kernel abortion. J Exp Bot 69:1599–1613CrossRefGoogle Scholar
  35. Turc O, Bouteillé M, Fuad-Hassan A, Welcker C, Tardieu F (2016) The growth of vegetative and reproductive structures (leaves and silks) respond similarly to hydraulic cues in maize. New Phytol 212:377–388CrossRefGoogle Scholar
  36. Ueguchi-Tanaka M, Ashikari M, Nakajima M, Itoh H, Katoh E, Kobayashi M, Chow T, Hsing YC, Kitano H, Yamaguchi I, Matsuoka M (2005) Gibberellin insensitive DWARF1 encodes a soluble receptor for gibberellin. Nature 437:693–698CrossRefGoogle Scholar
  37. Ventura L, Dona M, Macovei A, Carbonera D, Buttafava A, Mondoni A, Rossi G, Balestrazzi A (2012) Understanding the molecular pathways associated with seed vigor. Plant Physiol Bioch 60:196–206CrossRefGoogle Scholar
  38. White CN, Proebsting WM, Hedden P, Rivin CJ (2000) Gibberellins and seed development in maize. I. evidence that gibberellin/abscisic acid balance governs germination versus maturation pathways. Plant Physiol 122:1081–1088CrossRefGoogle Scholar
  39. Wu X, Liu H, Wang W, Chen S, Hu X, Li C (2010) Proteomic analysis of seed viability in maize. Acta Physiol Plant 33:181–191CrossRefGoogle Scholar
  40. Xie C, Mao X, Huang J, Ding Y, Wu J, Dong S, Kong L, Gao G, Li CY, Wei L (2011) KOBAS 2.0: a web server for annotation and identification of enriched pathways and diseases. Nucleic Acids Res 39:W316–W322CrossRefGoogle Scholar
  41. Yamaguchi S (2008) Gibberellin metabolism and its regulation. Annu Rev Plant Biol 59:225–251CrossRefGoogle Scholar
  42. Yang P, Li X, Wang X, Chen H, Chen F, Shen S (2007) Proteomic analysis of rice (Oryza sativa) seeds during germination. Proteomics 7:3358–3368CrossRefGoogle Scholar
  43. Young MD, Wakefield MJ, Smyth GK, Oshlack A (2010) Gene ontology analysis for RNA-seq: accounting for selection bias. Genome Biol 11:R14CrossRefGoogle Scholar
  44. Zhou Y, Chu P, Chen H, Li Y, Liu J, Ding Y, Tsang EW, Jiang L, Wu K, Huang S (2012) Overexpression of Nelumbo nucifera metallothioneins 2a and 3 enhances seed germination vigor in Arabidopsis. Planta 235:523–537CrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  1. 1.State Key Laboratory of Crop Biology, Agronomy CollegeShandong Agricultural UniversityTaianChina

Personalised recommendations