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Front. Plant Sci. | doi: 10.3389/fpls.2019.01505

How Does the Seed Pre-germinative Metabolism Fight against Imbibition Damage? Emerging Roles of Fatty Acid Cohort and Antioxidant Defence

Enrico Doria1,  Andrea Pagano1, 2,  Carla Ferreri3, Anna Vita Larocca4,  Anca Macovei1,  Susana Araújo5 and  Alma Balestrazzi1*
  • 1Department of Biology and Biotechnology Lazzaro Spallanzani, University of Pavia, Italy
  • 2Institute of Plant Genetics (PAN), Poland
  • 3Consiglio Nazionale delle Ricerche (Bologna), Italy
  • 4Lipinutragen Srl, Italy
  • 5Institute of Chemical and Biological Technology, New University of Lisbon, Portugal

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.

Keywords: Pre-germinative metabolism, Imbibition damage, lipidomics, antioxidant response, Medicago truncatula

Received: 02 Aug 2019; Accepted: 29 Oct 2019.

Copyright: © 2019 Doria, Pagano, Ferreri, Larocca, Macovei, Araújo and Balestrazzi. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

* Correspondence: Prof. Alma Balestrazzi, Department of Biology and Biotechnology Lazzaro Spallanzani, University of Pavia, Pavia, 27100, Lombardy, Italy, alma.balestrazzi@unipv.it