Cited by 42Seed Germination and PhysiologyPlant Stress Responses and ToleranceLipid metabolism and biosynthesis

How does the seed pre-germinative metabolism fight against imbibition damage? Emerging roles of fatty acid cohort and antioxidant defence.

Open access
Doria, Enrico, Pagano, Andrea, Ferreri, Carla, Larocca, Anna Vita, Macovei, Anca, Araújo, Susana de Sousa, Balestrazzi, Alma·2019·Frontiers in Plant Science

Abstract

During seed imbibition, lipids are engaged in membrane reorganization while facing free radical-mediated oxidative injury. In the present work, we explored changes in lipid components at different timepoints of imbibition (0.5, 2, 4, 6, and 8 h) in the legume Medicago truncatula, by combining biochemical approaches with targeted lipidomics and untargeted metabolomics. ROS and RNS (reactive oxygen and nitrogen species) accumulation was observed throughout the tested timepoints whereas lipid peroxidation increased at 4 h of imbibition. The seed response to oxidative damage was evidenced by a significant increase in tocopherols starting from 0.5 h of imbibition as well as by the reduction in total thiol content occurring at 2 h of imbibition. Since under physiological conditions, the proper functions of the cell membranes are strongly dependent on the qualitative and quantitative balance of fatty acid residues in phospholipids, the investigation was expanded to the fatty acid cohort of Medicago truncatula seeds. Total saturated fatty acids (SFAs), monounsaturated fatty acids (MUFAs), polyunsaturated fatty acids (PUFAs), omega-3 and omega-6 fatty acids showed fluctuations during seed imbibition. The most remarkable finding was the profile of the omega-3 PUFA docosopentaenoic acid (DPA, 7 cis, 10 cis, 13 cis, 16 cis, 19 cis-22:5) that showed a peak (up to 1.0% of the total fatty acid content) at 0.5 and 8 h of imbibition, respectively, concomitant with the peaks observed in tocopherol levels. It is possible that the observed changes in DPA alter the physical properties of membranes, as reported in animal cells, triggering signaling pathways relevant for the cell defence against oxidative injury. Furthermore, the content and balance between tocopherols and PUFAs is regarded as a determinant of storage stability. No enhancement in trans-fatty acids occurred throughout imbibition, suggesting for a proper antioxidant response carried by the seed. Fatty acids profiles were integrated with data from untargeted metabolomics showing changes in lipid sub-pathways, among which fatty acid amide, lyso-phospholipids and phospholipid metabolism. The emerging lipid profiles and dynamics are discussed in view of the overall imbibition damage generated during M. truncatula seed imbibition.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.3389/fpls.2019.01505

Cites

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Cites

No references could be resolved yet.

Research works printed but not linked: 62

  1. Ali A. A. Coulter J. A. Ogle C. H. Migaud M. M. Hirst D. G. Robson T. (2013). The contribution of N2O3 to the cytotoxicity of the nitric oxide donor DETA/NO: an emerging role for S-nytrosylation. Biosci. Rep. 33, e00031. 10.1042/BSR20120120 23402389 PMC3610299 · DOI
  2. Andreou A. Feussner I. (2009). Lipoxygenases - structure and reaction mechanism. Phytochem 70, 1504– 1510. 10.1016/j.phytochem.2009.05.008 19767040 · DOI
  3. Arc E. Galland M. Cueff G. Godin B. Lounifi I. Job D. (2011). Reboot the system thanks to protein post-translational modifications and proteome diversity: how quiescent seeds restart their metabolism to prepare seedling establishment. Proteomics 11, 1606– 1618. 10.1002/pmic.201000641 21433284 · DOI
  4. Bailly C. Maarouf-Bouteau H. Corbineau F. (2008). From intracellular signaling networks to cell death: the dual role of reactive oxygen species in seed physiology. C.R. Biol. 331, 806– 814. 10.1016/j.crvi.2008.07.022 18926495 · DOI
  5. Bewley J. D. (1997). Seed germination and dormancy. Plant Cell 9, 1055– 1066. 10.1105/tpc.9.7.1055 12237375 PMC156979 · DOI
  6. Bradford K. J. Benech-Arnold R. L. Come D. Corbineau F. (2008). Quantifying the sensitivity of barley seed germination to oxygen, abscisic acid, and gibberellin using a population-based threshold model. J. Exp. Bot. 59, 335– 347. 10.1093/jxb/erm315 18209108 · DOI
  7. Browse J. (2009). Jasmonate passes muster: a receptor and targets for the defense hormone. Annu. Rev. Plant Biol. 60, 183– 205. 10.1146/annurev.arplant.043008.092007 19025383 · DOI
  8. Chatgilialoglu C. Ferreri C. Ballestri M. Mulazzani Q. G. Landi L. (2000). cis-trans isomerization of monounsaturated fatty acids residues in phospholipids by thiyl radicals. J. Am. Chem. Soc 122, 4593– 4601. 10.1016/S0891-5849(02)01143-7 11457231 · DOI
  9. Chatgilialoglu C. Ferreri C. Masi A. Melchiorre M. Sansone A. Terzidis M. A. (2012). Biomimetic models of radical stress and related biomarkers. Chimia (Aarau) 66, 368– 371. 10.2533/chimia.2012.368 22871276 · DOI
  10. Chatgilialoglu C. Ferreri C. Melchiorre M. Sansone A. Torreggiani A. (2014). Lipid geometrical isomerism: from chemistry to biology and diagnostics. Chem. Rev. 114, 255– 284. 10.1021/cr4002287 24050531 · DOI
  11. Dave A. Graham I. A. (2012). Oxylipin signaling: a distinct role for the jasmonic acid precursor cis-(+)-12-oxo-phytodienoic acid (cis-OPDA). Front. Plant Sci. 3, 42. 10.3389/fpls.2012.00042 22645585 PMC3355751 · DOI
  12. Dave A. Hernandez M. L. He Z. Andriotis V. M. E. Vaistij F. E. Larson T. R. (2011). 2-oxo-phytodienoic acid accumulation during seed development represses seed germination in Arabidopsis. Plant Cell 23, 583– 599. 10.1105/tpc.110.081489 21335376 PMC3077774 · DOI
  13. Devaiah S. P. Pan X. Hong Y. Roth M. Welti R. Wang X. (2007). Enhancing seed quality and viability by suppressing phospholipase D in Arabidopsis. Plant J. 50, 950– 957. 10.1111/j.1365-313X.2007.03103.x 17565616 · DOI
  14. Djemel N. Guedon D. Lechevalier A. Salon C. Miquel M. Prosperi J. M. (2005). Development and composition of the seeds of nine genotypes of the Medicago truncatula species complex. Plant Physiol. Biochem. 43, 557– 566. 10.1016/j.plaphy.2005.04.005 15967671 · DOI
  15. Doria E. Galleschi L. Calucci L. Pinzino C. Pilu R. Cassani E. (2009). Phytic acid prevents oxidative stress in seeds: evidence from a maize (Zea mays L.) low phytic acid mutant. J. Exp. Bot. 60, 967– 978. 10.1093/jxb/ern345 19204030 · DOI
  16. Eldho N. V. Feller S. E. Tristram-Nagle S. Polozov I. V. Gawrisch K. (2003). Polyunsaturated docosahexaenoic vs docosapentaenoic acid-Differences in lipid matrix properties from the loss of one double bond. J. Am. Chem. Soc 12521, 6409– 6421. 10.1021/ja029029o 12785780 · DOI
  17. Evans A. M. Dehaven C. D. Barrett T. Mitchel M. Milgram E. (2009). Integrated, nontargeted ultrahigh performance liquid chromatography/electrospray ionization tandem mass spectrometry platform for the identification and relative quantification of the small molecule complement of biological systems. Anal. Chem. 81, 6650– 6667. 10.1021/ac901536h 19624122 · DOI
  18. Fahad S. Bajwa A. A. Nazir U. Anjum S. A. Farooq A. Zohaib A. (2017). Crop production under drought and heat stress: plant responses and management options. Front. Plant Sci. 8, 1147. 10.3389/fpls.2017.01147 28706531 PMC5489704 · DOI · Paper page
  19. Fan J. Yu L. Xu C. (2017). A central role for triacylglycerol in membrane lipid breakdown fatty acid ß-oxidation, and plant survival under extended darkness. Plant Physiol. 174, 1517– 1530. 10.1104/pp.17.00653 28572457 PMC5490926 · DOI
  20. Ferreri C. Masi A. Sansone A. Giacometti G. Larocca A. V. Menounou G. (2017). Fatty acids in membrane as homeostatic, metabolic and nutritional biomarkers: recent adavances in analytics and diagnostics. Diagn. (Basel) 7, 1. 10.3390/diagnostics7010001 PMC5373010 28025506 · DOI
  21. Hu K.-D. Hu L.-Y. Zhang F.-Q. Zhang H. (2007). Protective roles of nitric oxide on germination and antioxidant metabolism in wheat seeds under copper stress. Plant Growth Regul. 53, 173– 183. 10.1007/s10725-007-9216-9 · DOI
  22. Huang L. Grunwald C. (1990). Lipid and fatty acid changes during germination of alfalfa seeds. Phytochemistry 29, 1441– 1445. 10.1016/0031-9422(90)80097-Z · DOI
  23. Iqbal M. Iqbal Raja N. Yasmeen F. Hussain M. Ejaz M. Shah M. A. (2017). Impacts of heat stress on wheat: a critical review. Adv. Crop Sci. Tech. 5, 1. 10.4172/2329-8863.1000251 · DOI
  24. Ishibashi Y. Koda Y. Zheng S.-H. Yuasa T. Iwaya-Inoue M. (2013). Regulation of soybean seed germination through ethylene production in response to reactive oxygen species. Ann. Bot. 111, 95– 102. 10.1093/aob/mcs240 23131300 PMC3523653 · DOI
  25. Jouhet J. (2013). Importance of the hexagonal lipid phase in biological membrane organization. Front. Plant Sci. 4, 494. 10.3389/fpls.2013.00494 24348497 PMC3848315 · DOI
  26. Keereetaweep J. Blancaflor E. B. Hornung E. Feussner I. Chapman K. D. (2013). Ethanolamide oxylipins of linolenic acid can negatively regulate Arabidopsis seedling development. Plant Cell 25, 3824– 3840. 10.1105/tpc.113.119024 24151297 PMC3877782 · DOI
  27. Keereetaweep J. Blancaflor E. B. Hornung E. Feussner I. Chapman K. D. (2015). Lipoxygenase-derived 9-hydro(pero)xides of linoleoylethanolamide interact with ABA signaling to arrest root development during Arabidopsis seedling establishment. Plant J. 82, 315– 327. 10.1111/tpj.12821 25752187 · DOI
  28. Kovach D. A. Bradford K. J. (1992). Imbibitional damage and desiccation tolerance of wild rice (Zizania palustris) seeds. J. Exp. Bot. 43, 747– 757. 10.1093/jxb/43.6.747 · DOI
  29. Kranner I. Grill D. (1993). Content of low-molecular-weight thiols during the imbibition of pea seeds. Physiol. Plant 88, 557– 562. 10.1111/j.1399-3054.1993.tb01371.x 28741765 · DOI
  30. Kurilich C. Juvik J. (1999). Quantification of carotenoid and tocopherol antioxidants in Zea mays. J. Agr. Food Chem. 47, 1948– 1955. 10.1021/jf981029d 10552476 · DOI
  31. Ma Z. Marsolais F. Bykova N. V. Igamberdiev A. U. (2016). Nitric oxide and reactive oxygen species mediate metabolic changes in barley seed embryo during germination. Front. Plant Sci. 7, 138. 10.3389/fpls.2016.00138 26909088 PMC4754656 · DOI
  32. Macovei A. Caser M. Donà M. Valassi A. Giovannini A. Carbonera D. (2016). Prolonged cold storage affects pollen viability and germination along with hydrogen peroxide and nitric oxide content in Rosa hybrida. Not. Bot. Horti. Agro. 44, 6– 10. 10.15835/nbha44110357 · DOI
  33. Mansilla M. C. Cybulski L. E. Albanesi D. de Mendoza D. (2004). Control of membrane lipid fluidity by molecular thermosensors. J. Bacteriol. 186, 6681– 6688. 10.1128/JB.186.20.6681-6688.2004 15466018 PMC522199 · DOI
  34. Mene-Saffrane L. Dubugnon L. Chetelat A. Stolz S. Gouhier-Darimont C. Farmer E. E. (2009). Nonenzymatic oxidation of trienoic fatty acids contributes to reactive oxygen species management in Arabidopsis. J. Biol. Chem. 284, 1702– 1708. 10.1074/jbc.M807114200 18996838 · DOI
  35. Meyer C. J. Steudle E. Peterson C. A. (2007). Patterns and kinetics of water uptake by soybean seeds. J. Exp. Bot. 58, 717– 732. 10.1093/jxb/erl244 17185739 · DOI
  36. Noblet A. Leymarie J. Bailly C. (2017). Chilling temperature remodels phospholipidome of Zea mays seeds during imbibition. Sci. Rep. 7, 8886. 10.1038/s41598-017-08904-z 28827663 PMC5566375 · DOI
  37. Oliver M. J. Guo L. Alexander D. C. Ryals J. A. Wone B. W. Cushman J. C. (2011). A sister group contrast using untargeted global metabolomic analysis delineates the biochemical regulation underlying desiccation tolerance in Sporobolus stapfianus. Plant Cell 23, 1231– 1248. 10.1105/tpc.110082800 21467579 PMC3101564 · DOI
  38. Pagano A. de Sousa Araújo S. Macovei A. Dondi D. Lazzaroni S. Balestrazzi A. (2019). Metabolic and gene expression hallmarks of seed germination uncovered by sodium butyrate in Medicago truncatula. Plant Cell Environ. 2018, 1– 11. 10.1111/pce.13342 29756644 · DOI
  39. Park M. P. Hasenstein K. H. (2016). Oxygen dependency of germinating Brassica seeds. Life Sci. Space Res. 8, 30– 37. 10.1016/j.Issr.2016.01.002 26948011 · DOI
  40. Planchet E. Kaiser W. M. (2006). Nitric oxide (NO) detection by DAF fluorescence and chemiluminescence: a comparison using abiotic and biotic NO sources. J. Exp. Bot. 57, 3043– 3055. 10.1093/jxb/erl070 16893978 · DOI
  41. Powell A. A. Oliveira M. D. A. Matthews S. (1986). The role of imbibition damage in determining the vigour of white and coloured seed lots of dwarf French bean (Phaseolus vulgaris). J. Exp. Bot. 57, 716– 722. 10.1093/jxb/37.5.716 · DOI
  42. Powell A. A. (1998). Seed improvement by selection and invigoration. Sci. Agric. 55, 126– 133. 10.1590/S0103-90161998000500023 · DOI
  43. Rajjou L. Debeaujon I. (2008). Seed longevity: survival and maintenance of high germination ability of dry seeds. C.R. Biol. 331, 796– 805. 10.1016/j.crvi.2008.07.021 18926494 · DOI
  44. Rajjou L. Duval M. Gallardo K. Catusse J. Bally J. Job C. (2012). Seed germination and vigor. Annu. Rev. Plant Biol. 63, 507– 533. 10.1146/annurev-arplant-042811-105550 22136565 · DOI
  45. Ruiz-Lopez N. Haslam R. P. Husher S. I. Napier J. A. Sayanova O. (2013). Reconstitution of EPA and DHA biosynthesis in Arabidopsis: Iterative metabolic engineering for the synthesis of n-3 LC-PUFAs in transgenic plants. Metab. Eng. 17, 30– 41. 10.1016/j.ymben.2013.03.001 23500000 PMC3650579 · DOI
  46. Sansone A. Melchiorre M. Chatgilialoglu C. Ferreri C. (2013). Hexadecenoic fatty acid isomers: a chemical biology approach for human plasma biomarker development. Chem. Res. Toxicol. 26, 1703– 1709. 10.1021/tx400287u 24083821 · DOI
  47. Sari A. Kursat M. Civelek S. (2012). Determination of MDA levels in the plant (some Salvia L. Taxa growing In Turkey). J. Drug Metabol. Toxicol. 20123, 3. 10.4172/2157-7609.1000117 · DOI
  48. Sattler S. E. Gilliland L. U. Magallanes-Lundback M. Pollard M. DellaPenna D. (2004). Vitamin E is essential for seed longevity and for preventing lipid peroxidation during germination. Plant Cell 16, 1419– 1432. 10.1105/tpc.021360 15155886 PMC490036 · DOI
  49. Scanferlato R. Bortolotti M. Sansone A. Chatgilialoglu C. Polito L. De Spirito M. (2019). Hexadecenoic fatty acid positional isomers and denovo PUFA synthesis in colon cancer cells. Int. J. Mol. Sci. 20, 832. 10.3390/ijms20040832 PMC6412212 30769921 · DOI
  50. Simontacchi M. Jasid S. Puntarulo S. (2004). Nitric oxide generation during early germination of sorghum seeds. Plant Sci. 167, 839– 847. 10.1016/j.plantsci.2004.05.028 · DOI
  51. Song Y. He L. Wang X.-D. Smith N. Wheeler S. Garg M. L. (2017). Regulation of carbon partitioning in the seed of the model legume medicago truncatula and medicago orbicularis: a comparative approach. Front. Plant Sci. 8, 2070. 10.3389/fpls.2017.02070 29312368 PMC5733034 · DOI
  52. Storey J. Tibshirani R. (2003). Statistical significance for genomewide studies. P.N.A.S. U.S.A. 100, 9440– 9445. 10.1073/pnas.1530509100 PMC170937 12883005 · DOI · Paper page
  53. Tian Y. Katsuki A. Romanazzi D. Miller M. R. Adams S. L. Miyashita K. (2017). Docosapentaenoic acid (22:5n-3) downregulates mRNA expression of pro-inflammatory factors in LPS-activated murine macrophage like RAW264.7 cells. J. Oleo Sci. 66, 1149– 1156. 10.5650/jos.ess17111 28924088 · DOI
  54. Tzeng Y.-Z. Hu C.-H. (2014). Radical-induced cis-trans isomerization of fatty acids: a theoretical study. J. Phys. Chem. A 118, 4554– 4564. 10.1021/jp50243 24911614 · DOI
  55. Voldrich M. Dupont D. Dobias J. Philippon J. (1995). HPLC determination of thiol-containing anti-browning additives in fruit and vegetable product. Lebensm.-Wiss. u.-Technol. 28, 213– 217. 10.1016/S0023-6438(95)91502-8 · DOI
  56. Woolfield H. K. Cazenave-Gassiot A. Haslam R. P. Gushina I. A. Wenk M. R. Harwood J. H. (2018). Using lipidomics to reveal details of lipid accumulation in developing seeds from oilseed rape (Brassica napus L.). B.B.A.-Mol. Cell. Biol. Lipids 1863, 339– 348. 10.1016/j.bbalip.2017.12.010 PMC5791847 29275220 · DOI
  57. Wulff A. Oliveira H. C. Saviani E. E. Salgado I. (2009). Nitrite reduction and superoxide-dependent nitric oxide degradation by Arabidopsis mitochondria: influence of external NAD(P)H dehydrogenases and alternative oxidase in the control of nitric oxide levels. Nitric. Oxide 21, 132– 139. 10.1016/j.niox.2009.06.003 19576290 · DOI
  58. Xia J. Wishart D. S. (2016). Using MetaboAnalyst 3.0 for comprehensive metabolomics data analysis. Curr. Protoc. Bioinf. 55, 14.10.1– 14.10.91. 10.1002/cpbi.11 27603023 · DOI
  59. Yu X. Li A. Li W. (2015). How membranes organize during seed germination: three patterns of dynamic lipid remodelling define chilling resistance and affect plastid biogenesis. Plant Cell Environ. 38, 1391– 1403. 10.1111/pce.12494 25474382 PMC4766844 · DOI
  60. Zeb A. Ullah F. (2016). A simple spectrophotometric method for the determination of thiobarbituric acid reactive substances in fried fast foods. J. Anal. Methods Chem. 2016, 1– 5. 10.1155/2016/9412767 PMC4830699 27123360 · DOI
  61. Zhi Y. Taylor M. C. Campbell P. M. Warden A. C. Shrestha P. El Tahchy A. (2017). Comparative lipidomics and proteomics of lipid droplets in the mesocarp and seed tissues of chinese tallow (Triadica sebifera). Front. Plant Sci. 8, 1339. 10.3389/fpls.2017.01339 28824675 PMC5541829 · DOI
  62. Zhou X.-R. Callahan D. L. Shrestha P. Liu Q. Petrie J. R. Singh S. P. (2014). Lipidomic analysis of Arabidopsis seed genetically engineered to contain DHA. Front. Plant Sci. 5, 419. 10.3389/fpls.2014.00419 25225497 PMC4150447 · DOI

Cited by

Sorted by citations

Authors
Doria, E., Pagano, A., Ferreri, C., Larocca, A. V., Macovei, A., Araújo, S. D. S., & Balestrazzi, A.
Affiliations
  • University of Pavia (IT)
  • Bologna Research Area (IT)
  • Instituto de Tecnologia Química e Biológica António Xavier (PT)
Corresponding author
Balestrazzi, Alma
Venue
Frontiers in Plant Science
Published
2019-11-21
Volume
10
Pages
1505-1505
ISSN
1664-462X (ISSN-L)
OpenAlex
W2989698631
Cited by
42
References
0
Citations by year
2026: 10 · 2025: 8 · 2024: 3 · 2023: 10 · 2022: 8 · 2021: 1 · 2020: 2
FWCI
2.03
Type
journal article
Language
en
Open access
Locations
  • Frontiers in Plant Science (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • Archivio istituzionale della ricerca (Alma Mater Studiorum Università di Bologna) (submittedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders
  • Fondazione Cariplo
  • Ministero dell’Istruzione, dell’Università e della Ricerca
Topics
  • Life Sciences › Agricultural and Biological Sciences › Plant Science › Seed Germination and Physiology
  • Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant Stress Responses and Tolerance
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Biochemistry › Lipid metabolism and biosynthesis
Keywords
seed imbibition, Medicago truncatula, seed germination, lipid peroxidation, reactive oxygen species, reactive nitrogen species, tocopherols, thiol content, docosapentaenoic acid, omega-3 polyunsaturated fatty acids, fatty acid composition, phospholipid metabolism, fatty acid amides, lysophospholipids, antioxidant defense

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review