Abstract
Morphogenesis is a critical stage for the successful seedling establishment, which relies on energy provided by seed storage. Lipids are utilized as the primary energy storage material in most seed plants. The significance of alterations in fatty acid composition for seed germination has been reported; however, the mechanism underlying fatty acid utilization during morphogenesis remains unclear. Thus, the variation of fatty acid composition in response to light and dark signals was investigated in different tissues during Astragalus membranaceus seedling morphogenesis. Major difference in cotyledon was observed in fully opened and expanded. Compared to dark, light induced α-C18:3, C14:0 and C16:1 increased by 28%, 54%, and 86%, and C18:1, C21:0 and C20:0 decreased by 38%, 35%, and 11%, respectively. It seemed that the weakening of very long-chain fatty acids elongation and the enhancement of the palmitic acid elongation pathway, may have contributed to the synthesis of polyunsaturated fatty acids. Moreover, the changes of α-C18:3 in plastid membrane were significantly related to that of cotyledons. In newly differentiated tissues, the proportion of C16:0 and C18:0 in dark continued to increase to 36% and 20% while α-C18:3 gradually decreased to 15%, respectively. However, the increase or decrease in light were both stopped on A3 in which its elongation was inhibited. Meanwhile, it contained higher level of C22:0 in light and C22:1 in dark. Beyond that, C20:0, C16:1 C21:0 and C23:0 in both light and dark remained unchanged before cotyledon unearthing, then markedly increased after unearthing. Thus, our results presented a novel pattern of variation of fatty acid composition, which was important for understanding seedling morphogenesis.
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs10725-023-01044-7/MediaObjects/10725_2023_1044_Fig1_HTML.png)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs10725-023-01044-7/MediaObjects/10725_2023_1044_Fig2_HTML.png)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs10725-023-01044-7/MediaObjects/10725_2023_1044_Fig3_HTML.png)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs10725-023-01044-7/MediaObjects/10725_2023_1044_Fig4_HTML.png)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs10725-023-01044-7/MediaObjects/10725_2023_1044_Fig5_HTML.png)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs10725-023-01044-7/MediaObjects/10725_2023_1044_Fig6_HTML.png)
Similar content being viewed by others
References
Arnon DI (1949) Copper enzymes in isolated chloroplasts. Polyphenoloxidase in Beta Vulgaris. Plant Physiol 24(1):1–15
Arsovski AA, Galstyan A, Guseman JM, Nemhauser JL (2012) Photomorphogenesis Arabidopsis Book 10(e0147):e0147
Batsale M, Bahammou D, Fouillen L, Mongrand S, Joubès J, Domergue F (2021) Biosynthesis and functions of very-long-chain fatty acids in the responses of plants to abiotic and biotic stresses. Cells-Basel 10(6):1284
Brown EA (1996) Fatty acid compositions in newly differentiated tissues of soybean seedlings. Jagricfood Chem 44(6):1395–1398
Cao JB, He LM, Nwafor CC, Qin LH, Zhang CY, Song YT, Rong H (2021) Ultrastructural studies of seed coat and cotyledon during rapeseed maturation. J Integr Agr 20(5):1239–1249
Chen JX, **ang YE, Chen XP, Huang BQ (2005) Study on extraction of photosynthetic pigments from phytoplankton by organic solvents. J **amen Univ 44
de Carvalho JC, de Carvalho Gonçalves JF, Fernandes AV, da Costa KC, de Lima E, Borges EE, Araújo WL, Nunes-Nesi A, Ramos MV, Rathinasabapathi B (2022) Reserve mobilization and the role of primary metabolites during the germination and initial seedling growth of rubber tree genotypes. Acta Physiol Plant 44(8):80
Denic V, Weissman JS (2007) A molecular caliper mechanism for determining very long-chain fatty acid length. Cell 130(4):663–677
Diggle CP, Pitt E, Roberts P, Trejdosiewicz LK, Southgate J (2000) N–3 and n–6 polyunsaturated fatty acids induce cytostasis in human urothelial cells independent of p53 gene function. J Lipid Res 41(9):1509–1515
Dong C-J, Cao N, Zhang Z-G, Shang Q-M (2016) Characterization of the fatty acid desaturase genes in cucumber: structure, phylogeny, and expression patterns. PLoS ONE 11(3):e0149917
Doss M, Oette K (1965) Rapid method for the preparation of fatty acid methyl esters for gas chromatographic analysis. Z Klin Chem Klin Biochem 3(4):125–129
Erbas S, Tonguc M, Karakurt Y, Sanli A (2016) Mobilization of seed reserves during germination and early seedling growth of two sunflower cultivars. J Appl Bot Food Qual 89. https://doi.org/10.5073/Jabfq.2016.089.028
Gajewska E, Bernat P, Długoński J, Skłodowska M (2012) Effect of nickel on membrane integrity, lipid peroxidation and fatty acid composition in wheat seedlings. J Agron Crop Sci 198(4):286–294
Gendreau E, Traas J, Desnos T, Grandjean O, Caboche M, Hofte H (1997b) Cellular basis of hypocotyl growth in Arabidopsis thaliana. Plant Physiol 114(1):295–305
Gommers CM, Monte E (2018) Seedling establishment: a dimmer switch-regulated process between dark and light signaling. Plant Physiol 176(2):1061–1074
He D, Damaris RN, Fu J, Tu J, Fu T, Chen X, Yi B, Yang P (2016) Differential molecular responses of rapeseed cotyledons to light and dark reveal metabolic adaptations toward autotrophy establishment. Front Plant Sci 7:e56947
Heng Y, Lin F, Jiang Y, Ding M, Yan T, Lan H, Zhou H, Zhao X, Xu D, Deng XW (2019) B-Box containing proteins BBX30 and BBX31, acting downstream of HY5, negatively regulate photomorphogenesis in Arabidopsis. Plant Physiol 180(1):497–508
Ivanova A, Ananieva K, Mishev K, Ananiev E (2012) Lipid composition in leaves and cotyledons of Cucurbita pepo L. (zucchini) during natural and induced senescence. Genet Plant Physiol 2(1/2):98–106
Jaleel CA, Manivannan P, Wahid A, Farooq M, Aljuburi HJ, Somasundaram R, Panneerselvam R (2009) Drought stress in plants: a review on morphological characteristics and pigments composition. Int J Agric Biology 11(1):100–105
Kachroo A, Lapchyk L, Fukushige H, Hildebrand D, Klessig D, Kachroo P (2003) Plastidial fatty acid signaling modulates salicylic acid–and jasmonic acid–mediated defense pathways in the Arabidopsis ssi2 mutant. Plant Cell 15(12):2952–2965
Kelly AA, Quettier AL, Shaw E, Eastmond PJ (2011) Seed storage oil mobilization is important but not essential for germination or seedling establishment in Arabidopsis. Plant Physiol 157(2):866–875. https://doi.org/10.1104/pp.111.181784
Kumar N, Gautam A, Dubey AK, Ranjan R, Pandey A, Kumari B, Singh G, Mandotra S, Chauhan PS, Srikrishna S (2019) GABA mediated reduction of arsenite toxicity in rice seedling through modulation of fatty acids, stress responsive amino acids and polyamines biosynthesis. Ecotoxicol Environ Saf 173:15–27
Kuryata V, Kuts B, Poprotska I, Golunova L, Baiurko N, Nikitchenko L, Frytsiuk V (2021) Effect of gibberellin and tebuconazole on the use of seed reserve oil by Zea mays L. seedlings under photomorphogenesis and scotomorphogenesis conditions. Mod Phytomorphology 15:117–120
Le Guédard M, Faure O, Bessoule J-J (2012) Early changes in the fatty acid composition of photosynthetic membrane lipids from Populus nigra grown on a metallurgical landfill. Chemosphere 88(6):693–698
Li M, Bahn SC, Guo L, Musgrave W, Berg H, Welti R, Wang X (2011) Patatin-related phospholipase pPLAIIIβ-induced changes in lipid metabolism alter cellulose content and cell elongation in Arabidopsis. Plant Cell 23(3):1107–1123
Liu Y, Liu J, Wu KX, Guo XR, Tang ZH (2018) A rapid method for sensitive profiling of bioactive triterpene and flavonoid from Astragalus mongholicus and Astragalus membranaceus by ultra-pressure liquid chromatography with tandem mass spectrometry. Journal of Chromatography B Analytical Technologies in the Biomedical and Life Sciences 1085 (2018):110
Llorente B, Martinez-Garcia JF, Stange C, Rodriguez-Concepcion M (2017) Illuminating colors: regulation of carotenoid biosynthesis and accumulation by light. Curr Opin Plant Biol 37:49
Mackender RO, Leech RM (1974) The galactolipid, phospholipid, and fatty acid composition of the chloroplast envelope membranes of Vicia faba L. Plant Physiol 53(3):496–502
Murphy DJ (1990) Storage lipid bodies in plants and other organisms. Prog Lipid Res 29(4):299
Murphy DJ, Stumpf PK (1979) Light-dependent induction of polyunsaturated fatty acid biosynthesis in greening cucumber cotyledons. Plant Physiol 63(2):328–335
Nan Y, Guo X, Yan W, Hu X, Ma Y, Ye Z, Wang H, Tang Z (2018) The inhibited seed germination by ABA and MeJA is associated with the disturbance of reserve utilizations in Astragalus membranaceus. J Plant Interact 13(1):388–397
Navari-Izzo F, Quartacci MF, Melfi D, Izzo R (2010) Lipid composition of plasma membranes isolated from sunflower seedlings grown under water-stress. Physiol Plant 87(4):508–514
Nobusawa T, Okushima Y, Nagata N, Kojima M, Sakakibara H, Umeda M (2013) Synthesis of very-long-chain fatty acids in the epidermis controls plant organ growth by restricting cell proliferation. PLoS Biol 11(4):e1001531
Paque S, Mouille G, Grandont L, Alabadí D, Gaertner C, Goyallon A, Muller P, Primard-Brisset C, Sormani R, Blázquez MA (2014) AUXIN BINDING PROTEIN1 links cell wall remodeling, auxin signaling, and cell expansion in Arabidopsis. Plant Cell 26(1):280–295
Pavlík M, Zemanová V, Pavlíková D, Kyjaková P, Hlavsa T (2016) Regulation of odd-numbered fatty acid content plays an important part in the metabolism of the hyperaccumulator Noccaea spp. adapted to oxidative stress. J Plant Physiol 208:94
Peiretti P (2011) Fatty acid content and chemical composition of vegetative parts of perilla (Perilla frutescens L.) after different growth lengths. No. RESEARCH
Quettier AL, Eastmond PJ (2009) Storage oil hydrolysis during early seedling growth. Plant Physiol Biochem 47(6):485–490
Reed JW, Wu M-F, Reeves PH, Hodgens C, Yadav V, Hayes S, Pierik R (2018) Three auxin response factors promote hypocotyl elongation. Plant Physiol 178(2):864–875
Rivera Casado NA, Montes Horcasitas MD, Rodríguez VR, Esparza García FJ, Pérez VJ, Ariza CA, Ferrera-Cerrato R, Gómez GO, Calva CG (2015) The fatty acid profile analysis of cyperus laxus used for phytoremediation of soils from aged oil spill-impacted sites revealed that this is a C18:3 plant species. PLoS ONE 10(10):e0140103
Rodríguezvillalón A, Gas E, Rodríguezconcepción M (1962) Colors in the dark: a model for the regulation of carotenoid biosynthesis in etioplasts. Lancet 2(7258):699
Roudier F, Gissot L, Beaudoin F, Haslam R, Michaelson L, Marion J, Molino D, Lima A, Bach L, Morin H (2010) Very-long-chain fatty acids are involved in polar auxin transport and developmental patterning in Arabidopsis. Plant Cell 22(2):364–375
Schmitt F-J, Renger G, Friedrich T, Kreslavski VD, Zharmukhamedov SK, Los DA, Kuznetsov VV, Allakhverdiev SI (2014) Reactive oxygen species: re-evaluation of generation, monitoring and role in stress-signaling in phototrophic organisms. Biochim et Biophys Acta (BBA)-Bioenergetics 1837(6):835–848
Shepherd T, Wynne Griffiths D (2006) The effects of stress on plant cuticular waxes. New Phytol 171(3):469–499
Shi H, Lyu M, Luo Y, Liu S, Li Y, He H, Wei N, Deng XW, Zhong S (2018) Genome-wide regulation of light-controlled seedling morphogenesis by three families of transcription factors. Proc Natl Acad Sci 115(25):6482–6487
Shimizu T, Masuda T (2021) The role of tetrapyrrole-and GUN1-dependent signaling on chloroplast biogenesis. Plants 10(2):196
Shokravi Z, Shokravi H, Atabani A, Lau WJ, Chyuan OH, Ismail AF (2022) Impacts of the harvesting process on microalgae fatty acid profiles and lipid yields: implications for biodiesel production. Renew Sustain Energy Rev 161:112410
Sullivan JA, Deng XW (2003) From seed to seed: the role of photoreceptors in Arabidopsis development. Dev Biol 260(2):289–297
Tonguç M, Elkoyunu R, Erbaş S, Karakurt Y (2012) Changes in seed reserve composition during germination and initial seedling development of saffl ower (Carthamus tinctorius L). Turkish J Biology 36(1):107–112
Upchurch RG (2008) Fatty acid unsaturation, mobilization, and regulation in the response of plants to stress. Biotechnol Lett 30(6):967–977
Verma G, Mishra S, Sangwan N, Sharma S (2015) Reactive oxygen species mediate axis-cotyledon signaling to induce reserve mobilization during germination and seedling establishment in Vigna radiata. J Plant Physiol 184:79–88
Volmer R, van der Ploeg K, Ron D (2013) Membrane lipid saturation activates endoplasmic reticulum unfolded protein response transducers through their transmembrane domains. Proc Natl Acad Sci 110(12):4628–4633
Vonarnim A, Deng XW (1996) Light control of seedling development [Review]. Annu Rev Plant Physiol Plant Mol Biol 47(47):215–243
Xue Z, Chen Z, Wang Y, Sun W (2023) Proteomic analysis reveals the association between the pathways of glutathione and α-linolenic acid metabolism and lanthanum accumulation in tea plants. Molecules 28(3):1124
Yadukrishnan P, Singh D, Ravindran N, Kushwaha AK, Job N, Rahul PV, Yadav A, Ramachandran H, Bhagavatula L, Datta S (2021) Hormones and light-regulated seedling development. Horm Plant Response :91–116
Yang N, Zhang Y, Liu J, Liu Y, Chen Q, Wang H, Guo X, Herppich WB, Tang Z (2020) Network during light-induced cotyledons opening and greening in Astragalus membranaceus. J Plant Interact 15(1):358–370
Yoshida S, Uemura M (1986) Lipid composition of plasma membranes and tonoplasts isolated from etiolated seedlings of mung bean (Vigna radiata L). Plant Physiol 82(3):807–812
Zemanová V, Pavlík M, Kyjaková P, Pavlíková D (2015) Fatty acid profiles of ecotypes of hyperaccumulator Noccaea caerulescens growing under cadmium stress. J Plant Physiol 180:27–34
Zheng H, Rowland O, Kunst L (2005) Disruptions of the Arabidopsis enoyl-CoA reductase gene reveal an essential role for very-long-chain fatty acid synthesis in cell expansion during plant morphogenesis. Plant Cell 17(5):1467–1481
Zheng G, Tian B, Zhang F, Tao F, Li W (2011a) Plant adaptation to frequent alterations between high and low temperatures: remodelling of membrane lipids and maintenance of unsaturation levels. Plant Cell Environ 34(9):1431–1442
Zheng W, Wang P, Zhang H, Zhou D (2011b) Photosynthetic characteristics of the cotyledon and first true leaf of castor (Ricinus communis L). Aust J Crop Sci 5(6):702–708
Zheng Y, Cui X, Su L, Fang S, Chu J, Gong Q, Yang J, Zhu Z (2017) Jasmonate inhibits COP1 activity to suppress hypocotyl elongation and promote cotyledon opening in etiolated Arabidopsis seedlings. Plant J 90(6):1144
Zhou X-R, Shrestha P, Yin F, Petrie JR, Singh SP (2013) AtDGAT2 is a functional acyl-CoA: diacylglycerol acyltransferase and displays different acyl-CoA substrate preferences than AtDGAT1. FEBS Lett 587(15):2371–2376
Zhukov AV (2018) Very long-chain fatty acids in composition of plant membrane lipids. Russ J Plant Physiol 65(6):784–800. https://doi.org/10.1134/S1021443718050187
Zienkiewicz A, Jiménez-López JC, Zienkiewicz K, Alché JDD, Rodríguez-García MI (2011) Development of the cotyledon cells during olive (Olea europaea L.) in vitro seed germination and seedling growth. Protoplasma 248(4):751–765
Funding
This work was supported by the Fundamental Research Funds for the Central Universities (2572020DY04).
Author information
Authors and Affiliations
Contributions
Zhonghua Tang and Hongzheng Wang conceived and designed the experiments; Nan Yang, Chen Chen and Bing Jiang performed the experiments; Nan Yang and Shaolian Yu analyzed the data; Nan Yang and Liben Pan contributed reagents/materials/analysis tools; Nan Yang wrote the paper.
Corresponding authors
Ethics declarations
Conflict of interest
The authors declare no conflict of interest.
Additional information
Communicated by Ravinder Kumar.
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Yang, N., Pan, L., Jiang, B. et al. Variation of fatty acid composition in different tissues during Astragalus membranaceus seedling morphogenesis. Plant Growth Regul 101, 585–597 (2023). https://doi.org/10.1007/s10725-023-01044-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10725-023-01044-7