Abstract
Key message
Seed germination rate and oil content can be regulated at theGDSL transcriptional level by eitherAtGDSL1 orBnGDSL1 inB. napus.
Abstract
Gly-Asp-Ser-Leu (GDSL)-motif lipases represent an important subfamily of lipolytic enzymes, which play important roles in lipid metabolism, seed development, abiotic stress, and pathogen defense. In the present study, two closely related GDSL-motif lipases, Brassica napus GDSL1 and Arabidopsis thaliana GDSL1, were characterized as functioning in regulating germination rate and seed oil content in B. napus. AtGDSL1 and BnGDSL1 overexpression lines showed an increased seed germination rate and improved seedling establishment compared with wild type. Meanwhile, the constitutive overexpression of AtGDSL1 and BnGDSL1 promoted lipid catabolism and decreased the seed oil content. While RNAi-mediated suppression of BnGDSL1 (Bngdsl1) in B. napus improved the seed oil content and decreased seed germination rate. Moreover, the Bngdsl1 transgenic seeds showed changes in the fatty acid (FA) composition, featuring an increase in C18:1 and a decrease in C18:2 and C18:3. The transcriptional levels of six related core enzymes involved in FA mobilization were all elevated in the AtGDSL1 and BnGDSL1 overexpression lines, but strongly suppressed in the Bngdsl1 transgenic line. These results suggest that improving the seed germination and seed oil content in B. napus could be achieved by regulating the GDSL transcriptional level.
Similar content being viewed by others
References
Ahmad A, Bhattacharya A, McDonald RA et al (2011) Heat shock protein 70 kDa chaperone/DnaJ cochaperone complex employs an unusual dynamic interface. Proc Natl Acad Sci USA 108:18966–18971
Akoh CC, Lee GC, Liaw YC, Huang TH, Shaw JF (2004) GDSL family of serine esterases/lipases. Prog Lipid Res 43:534–552
Al-Taweel K, Fernando WG, Brûlé-Babel AL (2014) Transcriptome profiling of wheat differentially expressed genes exposed to different chemotypes of Fusarium graminearum. Theor Appl Genet 127:1703–1718
BäUmlein H, Boerjan W, Nagy I, Bassfüner R, Van Montagu M, Inzé D, Wobus U (1991) A novel seed protein gene from Vicia faba is developmentally regulated in transgenic tobacco and Arabidopsis plants. Mol Genl Genet 225:459–467
Bradbeer JW (1988) Seed dormancy and germination. Springer, New York
Brick DJ, Brumlik MJ, Buckley JT, Cao JX, Davies PC, Misra S, Tranbarger TJ. Upton C (1995) A new family of lipolytic plant enzymes with members in rice, Arabidopsis and maize. FEBS Lett 377:475–480
Chen M, Du X, Zhu Y, Wang Z, Hua S, Li Z, Guo W, Zhang G, Peng J, Jiang L (2012) Seed fatty acid reducer acts downstream of gibberellin signalling pathway to lower seed fatty acid storage in Arabidopsis. Plant Cell Environ 35:2155–2169
Chepyshko H, Lai CP, Huang LM, Liu JH, Shaw JF (2012) Multifunctionality and diversity of GDSL esterase/lipase gene family in rice (Oryza sativa L. japonica) genome: new insights from bioinformatics analysis. BMC Genom 13:309
Chia TY, Pike MJ, Rawsthorne S (2005) Storage oil breakdown during embryo development of Brassica napus (L.). J Exp Bot 5:1285–1296
Clauss K, von Roepenack-Lahaye E, Böttcher C et al (2011) Overexpression of sinapine esterase BnSCE3 in oilseed rape seeds triggers global changes in seed metabolism. Plant Physiol 155:1127–1145
Cruz Castillo M, Martinez C, Buchala A, Metraux JP, Leon J (2004) Gene-specific involvement of beta-oxidation in wound-activated responses in Arabidopsis. Plant Physiol 135:85–94
Dave A, Hernández 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 23:583–599
Ding L, Yang G, Cao J, Zhou Y, Yang R (2016)) Molecular cloning and functional characterization of a DNA damage-inducible (DDI) gene in Arabidopsis. Physiol Mol Plant Pathol 94:126–133
Eastmond PJ, Graham IA (2001) Re-examining the role of the glyoxylate cycle in oilseeds. Trends Plant Sci 6:72–78
El-Kouhen K, Blangy S, Ortiz E, Gardies AM, Ferte N, Arondel V (2005) Identification and characterization of a triacylglycerol lipase in Arabidopsis homologous to mammalian acid lipases. FEBS Lett 579:6067–6073
Ellinger D, Stingl N, Kubigsteltig II, Bals T, Juenger M, Pollmann S, Berger S, Schuenemann D, Mueller MJ (2010) DONGLE and DEFECTIVE IN ANTHER DEHISCENCE1 lipases are not essential for wound- and pathogen-induced jasmonate biosynthesis: redundant lipases contribute to jasmonate formation. Plant Physiol 153:114–127
Finch-Savage WE, Clay HA, Lynn JR, Morris K (2010) Towards a genetic understanding of seed vigour in small-seeded crops using natural variation in Brassica oleracea. Plant Sci 179:582–589
Finkelstein RR, Gampala SS, Rock CD (2002) Abscisic acid signaling in seeds and seedlings. Plant Cell 14:S15–S45
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 157:866–875
Kelly AA, Shaw E, Powers SJ, Kurup S, Eastmond PJ (2013) Suppression of the SUGAR-DEPENDENT1 triacylglycerol lipase family during seed development enhances oil yield in oilseed rape (Brassica napus L.). Plant Biotechnol J 11:355–361
Knauer S, Holt AL, Rubio-Somoza I et al (2013) A protodermal miR394 signal defines a region of stem cell competence in the Arabidopsis shoot meristem. Dev Cell 24:125–132
Koornneef M, Bentsink L, Hilhorst H (2002) Seed dormancy and germination. Curr Opin Plant Biol 5:33–36
Kucera B, Cohn MA, Leubner-Metzger G (2005) Plant hormone interactions during seed dormancy release and germination. Seed Sci Res 15:281–307
Li-Beisson Y, Shorrosh B, Beisson F et al (2010) Acyl-lipid metabolism. Arabidopsis Book 8:e0133
Ling H, Zhao J, Zuo K, Qiu C, Yao H, Qin J, Sun X, Tang K (2006) Isolation and expression analysis of a GDSL-like lipase gene from Brassica napus L. J Biochem Mol Biol 39:297
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2–∆∆CT T method. Methods 25:402–408
Mu J, Tan H, Zheng Q et al (2008) LEAFY COTYLEDON1 is a key regulator of fatty acid biosynthesis in Arabidopsis. Plant Physiol 148:10421054
Nesi N, Delourme R, Bregeon M, Falentin C, Renard M (2008) Genetic and molecular approaches to improve nutritional value of Brassica napus L. seed. C R Biol 331:763–771
Penfield S, Li Y, Gilday AD, Graham S, Graham IA (2006a) Arabidopsis ABA INSENSITIVE4 regulates lipid mobilization in the embryo and reveals repression of seed germination by the endosperm. Plant Cell 18:1887–1899
Penfield S, Pinfield-Wells HM, Graham IA (2006b) Storage reserve mobilisation and seedling establishment in Arabidopsis. Arabidopsis Book 4:e0100
Pinfield-Wells H, Rylott EL, Gilday AD, Graham S, Job K, Larson TR, Graham IA (2005) Sucrose rescues seedling establishment but not germination of Arabidopsis mutants disrupted in peroxisomal fatty acid catabolism. Plant J 43:861–872
Quettier AL, Eastmond PJ (2009) Storage oil hydrolysis during early seedling growth. Plant Physiol Biochem 47:485–490
Rombolá-Caldentey B, Rueda-Romero P, Iglesias-Fernández R, Carbonero P, Oñate-Sánchez L (2014) Arabidopsis DELLA and two HD-ZIP transcription factors regulate GA signaling in the epidermis through the L1 box cis-element. Plant Cell 26:2905–2919
Schaller A, Stintzi A (2009) Enzymes in jasmonate biosynthesis-structure, function, regulation. Phytochemistry 70:1532–1538
Schilmiller AL, Koo AJ, Howe GA (2007) Functional diversification of acyl-coenzyme A oxidases in jasmonic acid biosynthesis and action. Plant Physiol 143:812–824
Schmid M, Davison TS, Henz SR, Pape UJ, Demar M, Vingron M, Schölkopf B, Weigel D, Lohmann JU (2005) A gene expression map of Arabidopsis thaliana development. Nat Genet 37:501–506
Takahashi K, Shimada T, Kondo M, Tamai A, Mori M, Nishimura M, Hara-Nishimura I (2010) Ectopic expression of an esterase, which is a candidate for the unidentified plant cutinase, causes cuticular defects in Arabidopsis thaliana. Plant Cell Physiol 51:123–131
Tan H, Yang X, Zhang F et al (2011) Enhanced seed oil production in canola by conditional expression of Brassica napus LEAFY COTYLEDON1 and LEC1-LIKE in developing seeds. Plant Physiol 156:1577–1588
Upton C, Buckley JT (1995) A new family of lipolytic enzymes? Trends Biochem Sci 20:178–179
van Erp H, Kelly AA, Menard G, Eastmond PJ (2014) Multigene engineering of triacylglycerol metabolism boosts seed oil content in Arabidopsis. Plant Physiol 165:30–36
Wang H (2004) Strategy on the mid and long-term development of rapeseed variety improvement in China. Chin J Oil Crop Sci 26:98–101
Wang H (2010) Review and future development of rapeseed industry in China. Chin J Oil Crop Sci 2:023
Wang WC, Menon G, Hansen G (2003) Development of a novel Agrobacterium-mediated transformation method to recover transgenic Brassica napus plants. Plant Cell Rep 22:274–281
Wang Z, Fang H, Chen Y, Chen K, Li G, Gu S, Tan X (2014) Overexpression of BnWRKY33 in oilseed rape enhances resistance to Sclerotinia sclerotiorum. Mol Plant Pathol 15:677–689
Wasternack C, Hause B (2013) Jasmonates: biosynthesis, perception, signal transduction and action in plant stress response, growth and development. Ann Bot 111:1021–1058
Winter D, Vinegar B, Nahal H, Ammar R, Wilson GV, Provart NJ (2007) An “Electronic Fluorescent Pictograph” browser for exploring and analyzing large-scale biological data sets. PLoS One 2:e718
Xiang Y, Lu YH, Song M, Wang Y, Xu W, Wu L, Wang H, Ma Z (2015) Overexpression of a Triticum aestivum calreticulin gene TaCRT1 improves salinity tolerance in tobacco. PLoS One 10:e0140591
Acknowledgements
This work was supported by the National Key R&D Program of China (2016YFD0101904 and 2016YFD0100305) and the National Natural Science Foundation of China (31471527 and 31271760).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors have declared that no competing interests exist.
Additional information
Communicated by Hiroyasu Ebinuma.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Ding, LN., Guo, XJ., Li, M. et al. Improving seed germination and oil contents by regulating the GDSL transcriptional level in Brassica napus. Plant Cell Rep 38, 243–253 (2019). https://doi.org/10.1007/s00299-018-2365-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00299-018-2365-7