Re-modeling of foliar membrane lipids in a seagrass allows for growth in phosphorus-deplete conditions

Autoři: Jeremy P. Koelmel aff001;  Justin E. Campbell aff002;  Joy Guingab-Cagmat aff001;  Laurel Meke aff001;  Timothy J. Garrett aff001;  Ulrich Stingl aff003
Působiště autorů: University of Florida, Department of Pathology, Immunology, and Laboratory Medicine, College of Medicine, Gainesville, Florida, United States of America aff001;  Florida International University, Department of Biological Sciences, Institute of Water and Environment, North Miami, FL, United States of America aff002;  University of Florida, UF/IFAS Fort Lauderdale Research and Education Center, Department of Microbiology & Cell Science, Davie, Florida, United States of America aff003
Vyšlo v časopise: PLoS ONE 14(11)
Kategorie: Research Article
doi: 10.1371/journal.pone.0218690


In this study, we used liquid chromatography high-resolution tandem mass spectrometry to analyze the lipidome of turtlegrass (Thalassia testudinum) leaves with either extremely high phosphorus content or extremely low phosphorus content. Most species of phospholipids were significantly down-regulated in phosphorus-deplete leaves, whereas diacylglyceryltrimethylhomoserine (DGTS), triglycerides (TG), galactolipid digalactosyldiacylglycerol (DGDG), certain species of glucuronosyldiacylglycerols (GlcADG), and certain species of sulfoquinovosyl diacylglycerol (SQDG) were significantly upregulated, accounting for the change in phosphorus content, as well as structural differences in the leaves of plants growing across regions of varying elemental availability. These data suggest that seagrasses are able to modify the phosphorus content in leaf membranes dependent upon environmental availability.

Klíčová slova:

Cell membranes – Data acquisition – Fertilizers – Leaves – Lipid analysis – Lipid structure – Lipids – Phospholipids


1. Waycott M, Duarte CM, Carruthers TJB, Orth RJ, Dennison WC, Olyarnik S, et al. Accelerating loss of seagrasses across the globe threatens coastal ecosystems. PNAS. 2009;106: 12377–12381. doi: 10.1073/pnas.0905620106 19587236

2. Atkinson MJ, Smith SV. C:N:P ratios of benthic marine plants1. Limnology and Oceanography. 1983;28: 568–574. doi: 10.4319/lo.1983.28.3.0568

3. Duarte CM. Seagrass nutrient content. Marine Ecology Progress Series. 1990;67: 201–207.

4. Fourqurean JW, Zieman JC, Powell GVN. Phosphorus limitation of primary production in Florida Bay: Evidence from C:N:P ratios of the dominant seagrass Thalassia testudinum. Limnology and Oceanography. 1992;37: 162–171. doi: 10.4319/lo.1992.37.1.0162

5. Campbell JE, Altieri AH, Johnston LN, Kuempel CD, Paperno R, Paul VJ, et al. Herbivore community determines the magnitude and mechanism of nutrient effects on subtropical and tropical seagrasses. Van Alstyne K, editor. Journal of Ecology. 2018;106: 401–412. doi: 10.1111/1365-2745.12862

6. Barry SC, Jacoby CA, Frazer TK. Environmental influences on growth and morphology of Thalassia testudinum. Marine Ecology Progress Series. 2017;570: 57–70. doi: 10.3354/meps12112

7. The IUCN Red List of Threatened Species. In: IUCN Red List of Threatened Species [Internet]. [cited 28 Jan 2019]. Available:

8. Larkum AWD, Orth RJ, Duarte C, editors. Seagrasses: Biology, Ecology and Conservation [Internet]. Springer Netherlands; 2006. Available: //

9. Fourqurean JW, Jones RD, Zieman JC. Process Influencing Water Column Nutrient Characteristics and Phosphorus Limitation of Phytoplankton Biomass in Florida Bay, FL, USA:Inferences from Spatial Distributions. Estuarine, Coastal and Shelf Science. 1993;36: 295–314. doi: 10.1006/ecss.1993.1018

10. Armitage AR, Frankovich TA, Fourqurean JW. Long-Term Effects of Adding Nutrients to an Oligotrophic Coastal Environment. Ecosystems. 2011;14: 430–444. doi: 10.1007/s10021-011-9421-2

11. Fourqurean JW, Zieman JC, Powell GVN. Relationships between porewater nutrients and seagrasses in a subtropical carbonate environment. Marine Biology. 1992;114: 57–65. doi: 10.1007/BF00350856

12. Folch J, Lees M, Sloane Stanley GH. A simple method for the isolation and purification of total lipides from animal tissues. J Biol Chem. 1957;226: 497–509. 13428781

13. Pluskal T, Castillo S, Villar-Briones A, Orešič M. MZmine 2: Modular framework for processing, visualizing, and analyzing mass spectrometry-based molecular profile data. BMC Bioinformatics. 2010;11: 395. doi: 10.1186/1471-2105-11-395 20650010

14. Kirpich AS, Ibarra M, Moskalenko O, Fear JM, Gerken J, Mi X, et al. SECIMTools: a suite of metabolomics data analysis tools. BMC Bioinformatics. 2018;19: 151. doi: 10.1186/s12859-018-2134-1 29678131

15. Patterson RE, Kirpich AS, Koelmel JP, Kalavalapalli S, Morse AM, Cusi K, et al. Improved experimental data processing for UHPLC–HRMS/MS lipidomics applied to nonalcoholic fatty liver disease. Metabolomics. 2017;13: 142. doi: 10.1007/s11306-017-1280-1

16. Koelmel JP, Kroeger NM, Ulmer CZ, Bowden JA, Patterson RE, Cochran JA, et al. LipidMatch: an automated workflow for rule-based lipid identification using untargeted high-resolution tandem mass spectrometry data. BMC Bioinformatics. 2017;18: 331. doi: 10.1186/s12859-017-1744-3 28693421

17. Tsugawa H, Cajka T, Kind T, Ma Y, Higgins B, Ikeda K, et al. MS-DIAL: data-independent MS/MS deconvolution for comprehensive metabolome analysis. Nat Meth. 2015;12: 523–526. doi: 10.1038/nmeth.3393 25938372

18. R Development Core Team. R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing; 2016.

19. Xia J, Wishart DS. Metabolomic data processing, analysis, and interpretation using MetaboAnalyst. Curr Protoc Bioinformatics. 2011;Chapter 14: Unit 14.10. doi: 10.1002/0471250953.bi1410s34 21633943

20. Benjamini Y, Hochberg Y. Controlling the False Discovery Rate: A Practical and Powerful Approach to Multiple Testing. Journal of the Royal Statistical Society Series B (Methodological). 1995;57: 289–300.

21. LipidMatch Flow (Beta) [Internet]. [cited 28 Jan 2019]. Available:

22. Koelmel JP, Kroeger NM, Ulmer CZ, Bowden JA, Patterson RE, Cochran JA, et al. LipidMatch: an automated workflow for rule-based lipid identification using untargeted high-resolution tandem mass spectrometry data. BMC Bioinformatics. 2017;18: 331. doi: 10.1186/s12859-017-1744-3 28693421

23. Khotimchenko SV. Fatty acids and polar lipids of seagrasses from the sea of Japan. Phytochemistry. 1993;33: 369–372. doi: 10.1016/0031-9422(93)85520-2

24. Minnikin DE, Abdolrahimzadeh H, Baddiley J. Replacement of acidic phospholipids by acidic glycolipids in Pseudomonas diminuta. Nature. 1974;249: 268–269. doi: 10.1038/249268a0 4833243

25. Benning C. Biosynthesis and Function of the Sulfolipid Sulfoquinovosyl Diacylglycerol. Annual Review of Plant Physiology and Plant Molecular Biology. 1998;49: 53–75. doi: 10.1146/annurev.arplant.49.1.53 15012227

26. Essigmann B, Güler S, Narang RA, Linke D, Benning C. Phosphate availability affects the thylakoid lipid composition and the expression of SQD1, a gene required for sulfolipid biosynthesis in Arabidopsis thaliana. Proc Natl Acad Sci USA. 1998;95: 1950–1955. doi: 10.1073/pnas.95.4.1950 9465123

27. Van Mooy BAS, Fredricks HF, Pedler BE, Dyhrman ST, Karl DM, Koblížek M, et al. Phytoplankton in the ocean use non-phosphorus lipids in response to phosphorus scarcity. Nature. 2009;458: 69–72. doi: 10.1038/nature07659 19182781

28. Andersson MX, Stridh MH, Larsson KE, Liljenberg C, Sandelius AS. Phosphate-deficient oat replaces a major portion of the plasma membrane phospholipids with the galactolipid digalactosyldiacylglycerol. FEBS Lett. 2003;537: 128–132. doi: 10.1016/s0014-5793(03)00109-1 12606044

29. Tjellström H, Andersson MX, Larsson KE, Sandelius AS. Membrane phospholipids as a phosphate reserve: the dynamic nature of phospholipid-to-digalactosyl diacylglycerol exchange in higher plants. Plant Cell Environ. 2008;31: 1388–1398. doi: 10.1111/j.1365-3040.2008.01851.x 18643953

30. Riekhof WR, Naik S, Bertrand H, Benning C, Voelker DR. Phosphate starvation in fungi induces the replacement of phosphatidylcholine with the phosphorus-free betaine lipid diacylglyceryl-N,N,N-trimethylhomoserine. Eukaryotic Cell. 2014;13: 749–757. doi: 10.1128/EC.00004-14 24728191

31. Okazaki Y, Otsuki H, Narisawa T, Kobayashi M, Sawai S, Kamide Y, et al. A new class of plant lipid is essential for protection against phosphorus depletion. Nat Commun. 2013;4: 1510. doi: 10.1038/ncomms2512 23443538

32. Dean AP, Sigee DC, Estrada B, Pittman JK. Using FTIR spectroscopy for rapid determination of lipid accumulation in response to nitrogen limitation in freshwater microalgae. Bioresour Technol. 2010;101: 4499–4507. doi: 10.1016/j.biortech.2010.01.065 20153176

33. Hu Q, Sommerfeld M, Jarvis E, Ghirardi M, Posewitz M, Seibert M, et al. Microalgal triacylglycerols as feedstocks for biofuel production: Perspectives and advances. The Plant Journal. 2008;54: 621–639. doi: 10.1111/j.1365-313X.2008.03492.x 18476868

Článek vyšel v časopise


2019 Číslo 11