Skip to main content
SpringerLink
Log in

Overexpression of Heteromeric GhACCase Subunits Enhanced Oil Accumulation in Upland Cotton

  • Original Paper
  • Published:
Plant Molecular Biology Reporter Aims and scope Submit manuscript

Abstract

Acetyl-CoA carboxylase (ACCase) catalyzes acetyl-CoA to produce malonyl-CoA, which is the essential first step in the biosynthesis of de novo fatty acids. The heteromeric ACCase of higher plants, such as upland cotton, is composed of four subunits: biotin carboxyl carrier protein (BCCP), biotin carboxylase (BC), α-subunit of carboxyltransferase (CTα), and β-subunit of carboxyltransferase (CTβ). In this study, four subunits encoding heteromeric ACCase were amplified and the structures were analyzed further. The result showed that 7, 16, 10, and 1 exon(s) were identified from GhBCCP1, GhBC1, GhCTα2, and GhCTβ, respectively. The expression pattern analysis showed that the transcripts of these four subunits were ubiquitous in all the tested tissues and may have a positive correlation between the four subunits and oil accumulation. The four subunits coordinate to enhance oil content. The expression patterns and levels varied under ABA, MeJA treatments, and cold stress. Furthermore, under the control of a seed-specific AGP promoter, overexpression of the four subunits separately in Upland cotton demonstrated that GhBCCP1 transgenic plants showed a significant increase of 21.92% in oil content in cotton seeds, while about a 17% increase was noted for GhBC1 and GhCTβ, respectively. So overexpression of each subunit of heteromeric GhACCase may effectively increase seed oil content in Upland cotton.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Ahuja I, Vos RCHD, Bones AM et al (2010) Plant molecular stress responses face climate change. Trends Plant Sci 15:664–674

    Article  CAS  PubMed  Google Scholar 

  • Baud S, Lepiniec L (2009) Regulation of de-novo fatty acid synthesis in maturing oilseeds of Arabidopsis. Plant Physiol Bioch 47:448–455

    Article  CAS  Google Scholar 

  • Chen B, Wang J, Zhang G et al (2016) Two types of soybean diacylglycerol acyltransferases are differentially involved in triacylglycerol biosynthesis and response to environmental stresses and hormones. Scientific Reports 6:28541

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen M, Markham JE, Cahoon EB (2012) Sphingolipid Δ8 unsaturation is important for glucosylceramide biosynthesis and low-temperature performance in Arabidopsis. Plant J 69:769–781

    Article  CAS  PubMed  Google Scholar 

  • Choi JK, Yu F, Wurtele ES et al (1995) Molecular cloning and characterization of the cDNA coding for the biotin-containing subunit of the chloroplastic acetyl-coenzyme A carboxylase. Plant Physiol 109:619–625

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Davis MS, Solbiati J, Cronan JE (2000) Overproduction of acetyl-CoA carboxylase activity increases the rate of fatty acid biosynthesis in Escherichia coli. J Biol Chem 275:28593–28598

    Article  CAS  PubMed  Google Scholar 

  • Dong J, Wei LB, Hu Y et al (2013) Molecular cloning and characterization of three novel genes related to fatty acid degradation and their responses to abiotic stresses in Gossypium hirsutum L. J Integr Agric 12:582–588

    Article  Google Scholar 

  • Elborough KM, Winz R, Deka RK et al (1996) Biotin carboxyl carrier protein and carboxyltransferase subunits of the multi-subunit form of acetyl-CoA carboxylase from Brassica napus: cloning and analysis of expression during oilseed rape embryogenesis. Biochem J 315:103–112

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Erdei L, Stuiver B, Kuiper PJC (2006) The effect of salinity on lipid composition and on activity of Ca2+- and Mg2+-stimulated ATPases in salt-sensitive and salt-tolerant Plantago species. Physiol Plant 49:315–319

    Article  Google Scholar 

  • Flagella Z, Giuliani MM, Rotunno T et al (2004) Effect of saline water on oil yield and quality of a high oleic sunflower (Helianthus annuus L.) hybrid. Eur J Agron 21:267–272

    Article  Google Scholar 

  • Gu K, Chiam H, Tian D et al (2011) Molecular cloning and expression of heteromeric ACCase subunit genes from Jatropha curcas. Plant Sci 180:642–649

    Article  CAS  PubMed  Google Scholar 

  • Hamada T, Nishiuchi T, Kodama H et al (1996) cDNA cloning of a wounding-inducible gene encoding a plastid ω-3 fatty acid desaturase from tobacco. Plant Cell Physiol 37:606–611

    Article  CAS  PubMed  Google Scholar 

  • Heuer B, Yaniv Z, Ravina I (2002) Effect of late salinization of chia (Salvia hispanica) stock (Matthiola tricuspidata) and evening primrose (Oenothera biennis) on their oil content and quality. Ind Crop Prod 15:163–167

    Article  CAS  Google Scholar 

  • Hu B, Jin J, Guo A, Zhang H et al (2015) GSDS 20: an upgraded gene feature visualization server. Bioinformatics 31:1296–1297

    Article  PubMed  Google Scholar 

  • Islam MS, Fang DD, Thyssen GN et al (2016) Comparative fiber property and transcriptome analyses reveal key genes potentially related to high fiber strength in cotton (Gossypium hirsutum L.) line MD52ne. BMC Plant Biol 16:1–19

    Article  Google Scholar 

  • Ji SJ, Lu YC, Feng JX et al (2003) Isolation and analyses of genes preferentially expressed during early cotton fiber development by subtractive PCR and cDNA array. Nucl Acids Res 31:2534–2543

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kachroo A, Kachroo P (2009) Fatty acid-derived signals in plant defense. Annu Rev Phytopathol 47:153–176

    Article  CAS  PubMed  Google Scholar 

  • Ke J, Choi JK, Smith M et al (1997) Structure of the CAC1 gene and in situ characterization of its expression: the Arabidopsis thaliana gene coding for the biotin-containing subunit of the plastidic acetyl-coenzyme A carboxylase. Plant Physiol 113:357–365

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ke J, Wen TN, Nikolau BJ et al (2000) Coordinate regulation of the nuclear and plastidic genes coding for the subunits of the heteromeric acetyl-coenzyme A carboxylase. Plant Physiol 122:1057–1071

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Khodakovskaya M, McAvoy R, Peters J et al (2006) Enhanced cold tolerance in transgenic tobacco expressing a chloroplast ω-3 fatty acid desaturase gene under the control of a cold-inducible promoter. Planta 223:1090–1100

    Article  CAS  PubMed  Google Scholar 

  • Konishi T, Sasaki Y (1994) Compartmentalization of two forms of acetyl-CoA carboxylase in plants and the origin of their tolerance toward herbicides. Proc Natl Acad Sci U S A 91:3598–3601

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Konishi T, Shinohara K, Yamada K et al (1996) Acetyl-CoA carboxylase in higher plants: most plants other than gramineae have both the prokaryotic and the eukaryotic forms of this enzyme. Plant Cell Physiol 37:117–122

    Article  CAS  PubMed  Google Scholar 

  • Lee SB, Kaittanis C, Jansen RK et al (2006) The complete chloroplast genome sequence of Gossypium hirsutum: organization and phylogenetic relationships to other angiosperms. BMC Genomics 7:61

    Article  PubMed  PubMed Central  Google Scholar 

  • Li F, Fan G, Lu C et al (2015) Genome sequence of cultivated Upland cotton (Gossypium hirsutum TM-1) provides insights into genome evolution. Nat Biotechnol 33:524–530

    Article  PubMed  Google Scholar 

  • Li MJ, Xia H, Zhao CZ et al (2010a) Isolation and characterization of putative acetylCoA carboxylases in Arachis hypogaea L. Plant Mol Biol Report 28:58–68

    Article  CAS  Google Scholar 

  • Li X, Ilarslan H, Brachova L et al (2011a) Reverse-genetic analysis of the two biotin-containing subunit genes of the heteromeric acetyl-coenzyme A carboxylase in Arabidopsis indicates a unidirectional functional redundancy. Plant Physiol 155:293–314

    Article  CAS  PubMed  Google Scholar 

  • Li ZG, Yin WB, Guo H et al (2010b) Genes encoding the α-carboxyltransferase subunit of acetyl-CoA carboxylase from Brassica napus and parental species: cloning expression patterns and evolution. Genome 53:360–370

    Article  CAS  PubMed  Google Scholar 

  • Li ZG, Yin WB, Guo H et al (2011b) Genes encoding the biotin carboxylase subunit of acetyl-CoA carboxylase from Brassica napus and parental species: cloning expression patterns and evolution. Genome 54:202–211

    Article  PubMed  Google Scholar 

  • Li-Beisson Y, Shorrosh B, Beisson F et al (2010) Acyl-lipid metabolism. Arabidopsis Book 8:e0133

    Article  PubMed  PubMed Central  Google Scholar 

  • Liu F, Xia Y, Wu L et al (2015a) Enhanced seed oil content by overexpressing genes related to triacylglyceride synthesis. Gene 557:163–171

    Article  CAS  PubMed  Google Scholar 

  • Liu W, Li W, He Q et al (2015b) Characterization of 19 genes encoding membrane-bound fatty acid desaturases and their expression profiles in Gossypium raimondii under low temperature. PLoS One 10:e0123281

    Article  PubMed  PubMed Central  Google Scholar 

  • Liu Z, Zhang Y, Wang Y et al (2011) Construction of seed specific expression vectors and genetic transformation for genes of heteromeric ACCase in Upland cotton. Molecular Plant Breeding 9:270–277 (in Chinese)

    CAS  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2-△△CT method. Methods 25:402–408

    Article  CAS  PubMed  Google Scholar 

  • Luque-GarcíA JL, Castro MD (2004) Ultrasound-assisted Soxhlet extraction: an expeditive approach for solid sample treatment: application to the extraction of total fat from oleaginous seeds. J Chromatogr A 1034:237–242

    Article  PubMed  Google Scholar 

  • Madoka Y, Tomizawa K, Mizoi J et al (2002) Chloroplast transformation with modified accD operon increases acetyl-CoA carboxylase and causes extension of leaf longevity and increase in seed yield in tobacco. Plant Cell Physiol 43:1518–1525

    Article  CAS  PubMed  Google Scholar 

  • Mu M, Lu XK, Wang JJ et al (2016) Genome-wide identification and analysis of the stress-resistance function of the TPS (trehalose-6-phosphate synthase) gene family in cotton. BMC Genet 17:54

    Article  PubMed  PubMed Central  Google Scholar 

  • Nair PMG, Kang IS, Moon BY et al (2009) Effects of low temperature stress on rice (Oryza sativa L.) plastid ω-3 desaturase gene OsFAD8 and its functional analysis using T-DNA mutants. Plant Cell Tiss Organ Cult 98:87–96

    Article  CAS  Google Scholar 

  • Ohlrogge J, Browse J (1995) Lipid biosynthesis. Plant Cell 7:957–970

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Parti RS, Deep V, Gupta SK (2003) Effect of salinity on lipid components of mustard seeds (Brassica juncea L.). Plant Foods Hum Nutr 58:1–10

    Article  Google Scholar 

  • Pidkowich MS, Nguyen HT, Heilmann I et al (2007) Modulating seed beta-ketoacyl-acyl carrier protein synthase II level converts the composition of a temperate seed oil to that of a palm-like tropical oil. Proc Natl Acad Sci U S A 104:4742–4747

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Puyaubert J, Garcia C, Chevalier S et al (2005) Acyl-CoA elongase a key enzyme in the development of high-erucic acid rapeseed? Eur J Lipid Sci Technol 107:263–267

    Article  CAS  Google Scholar 

  • Qayyum MA, Malik D (1988) Farm production losses in salt affected soils. In managing soil resources proc. 1st Nat Cong On soil Sci. Lahore, pp 356–364

  • Qiao ZX, Liu JY (2007) Cloning and characterization of cotton heteromeric acetyl-CoA carboxylase genes. Prog Nat Sci 17:1412–1418

    CAS  Google Scholar 

  • Qin YM, Hu CY, Pang Y et al (2007) Saturated very-long-chain fatty acids promote cotton fiber and Arabidopsis cell elongation by activating ethylene biosynthesis. Plant Cell 19:3692–3704

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ran H, Faigenboimdoron A, Kadmon N et al (2015) A transcriptome profile for developing seed of polyploid cotton. Plant Genome 8:1–15

    Google Scholar 

  • Reverdatto S, Beilinson V, Nielsen NC (1999) A multisubunit acetyl coenzyme A carboxylase from soybean. Plant Physiol 119:961–978

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Román Á, Andreu V, Hernández ML et al (2012) Contribution of the different omega-3 fatty acid desaturase genes to the cold response in soybean. J Exp Bot 63:4973–4982

    Article  PubMed  PubMed Central  Google Scholar 

  • Sasaki Y, Hakamada K, Suama Y et al (1993) Chloroplast-encoded protein as a subunit of acetyl-CoA carboxylase in pea plant. J Biol Chem 268:25118–25123

    CAS  PubMed  Google Scholar 

  • Sasaki Y, Konishi T, Nagano Y (1995) The compartmentation of acetyl-coenzyme A carboxylase in plants. Plant Physiol 108:445–449

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sasaki Y, Nagano Y (2004) Plant acetyl-CoA carboxylase: structure, biosynthesis, regulation, and gene manipulation for plant breeding. Biosci Biotechnol Biochem 68:1175–1184

    Article  CAS  PubMed  Google Scholar 

  • Seki M, Kamei A, Yamaguchi-Shinozaki K et al (2003) Molecular responses to drought salinity and frost: common and different paths for plant protection. Curr Opin Biotechnol 14:194–199

    Article  CAS  PubMed  Google Scholar 

  • Shang L, Abduweli A, Wang Y et al (2016) Genetic analysis and QTL mapping of oil content and seed index using two recombinant inbred lines and two backcross populations in upland cotton. Plant Breed 135:224–231

    Article  CAS  Google Scholar 

  • Shang L, Li J, Wang Y et al (2015) Establishment and application of model for determining oil content of cottonseed using near infrared spectroscopy. Spectrosc Spectr Anal 35:609–612 (in Chinese)

    CAS  Google Scholar 

  • Shi G, Guo X, Guo J et al (2015) Analyzing serial cDNA libraries revealed reactive oxygen species and gibberellins signaling pathways in the salt response of Upland cotton (Gossypium hirsutum L.). Plant Cell Rep 34:1005–1023

    Article  CAS  PubMed  Google Scholar 

  • Shorrosh BS, Roesler KR, Shintani D et al (1995) Structural analysis plastid localization and expression of the biotin carboxylase subunit of acetyl-coenzyme A carboxylase from tobacco. Plant Physiol 108:805–812

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thelen JJ, Mekhedov S, Ohlrogge JB (2001) Brassicaceae express multiple isoforms of biotin carboxyl carrier protein in a tissue-specific manner. Plant Physiol 125:2016–2028

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Troncoso-Ponce MA, Kilaru A, Cao X et al (2011) Comparative deep transcriptional profiling of four developing oilseeds. Plant J 68:1014–1027

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Upchurch RG (2008) Fatty acid unsaturation mobilization and regulation in the response of plants to stress. Biotechnol Lett 30:967–977

    Article  CAS  PubMed  Google Scholar 

  • Wang HS, Yu C, Tang XF et al (2014) A tomato endoplasmic reticulum (ER)-type omega-3 fatty acid desaturase (LeFAD3) functions in early seedling tolerance to salinity stress. Plant Cell Rep 33:131–142

    Article  CAS  PubMed  Google Scholar 

  • Wanjie SW, Welti R, Moreau RA et al (2005) Identification and quantification of glycerolipids in cotton fibers: reconciliation with metabolic pathway predictions from DNA databases. Lipids 40:773–785

    Article  CAS  PubMed  Google Scholar 

  • Wolter FP, Schmidt R, Heinz E (1992) Chilling sensitivity of Arabidopsis thaliana with genetically engineered membrane lipids. EMBO J 11:4685–4692

    CAS  PubMed  PubMed Central  Google Scholar 

  • Xuan W, Zhang Y, Liu ZQ et al (2015) Molecular cloning and expression analysis of a novel BCCP subunit gene from Aleurites moluccana. Genet Mol Res 14:9922–9931

    Article  CAS  PubMed  Google Scholar 

  • Zhang J, Liu H, Sun J et al (2012) Arabidopsis fatty acid desaturase FAD2 is required for salt tolerance during seed germination and early seedling growth. PLoS One 7:e30355

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang JT, Zhu JQ, Zhu Q et al (2009) Fatty acid desaturase-6 (Fad6) is required for salt tolerance in Arabidopsis thaliana. Biochem Biophys Res Commun 390:469–474

    Article  CAS  PubMed  Google Scholar 

  • Zhang T, Hu Y, Jiang W et al (2015) Sequencing of allotetraploid cotton (Gossypium hirsutum acc TM-1) provides a resource for fiber improvement. Nat Biotech 33:531–537

    Article  CAS  Google Scholar 

  • Zhou G, Weng J, Zeng Y et al (1983) Introduction of exogenous DNA into cotton embryos. Methods Enzymol 101:433–481

    Article  CAS  PubMed  Google Scholar 

  • Zou J, Abrams GD, Barton DL et al (1995) Induction of lipid and oleosin biosynthesis by (+) -abscisic acid and its metabolites in microspore-derived embryos of Brassica napus L cv Reston (biological responses in the presence of 8′ [prime]-hydroxyabscisic acid). Plant Physiol 108:563–571

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

The work was supported by grants from the National Natural Science Foundation of China (Grant No. 31371666).

Author information

Author notes

  1. Zhengjie Liu

    Present address: College of Agriculture and Biotechnology, Yunnan Agricultural University, Kunming, Yunnan, 650201, China

Authors and Affiliations

  1. Laboratory of Cotton Genetics, Genomics and Breeding, College of Agronomy and Biotechnology/Beijing Key Laboratory of Crop Genetic Improvement, China Agricultural University, Beijing, 100193, China

    Yupeng Cui, Zhengjie Liu, Yanpeng Zhao, Le Li, Han Wu, Suixi Xu & Jinping Hua

  2. Research Institute of Cash Crops, Hubei Academy of Agricultural Sciences, Wuhan, Hubei, 430064, China

    Yumei Wang

  3. Oil Crops Research Institute, Chinese Academy of Agricultural Sciences, Wuhan, Hubei, 430062, China

    Yi Huang

Authors
  1. Yupeng Cui
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Zhengjie Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yanpeng Zhao
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Yumei Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Yi Huang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Le Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Han Wu
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Suixi Xu
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Jinping Hua
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jinping Hua.

Electronic supplementary material

Fig. S1

Expression patterns of GhBCCP1, GhBC1, GhCTα2, and GhCTβ in different tissues of ‘Sumian 20’. Total RNAs were isolated from root (R), stem (S), leaf (L) and fiber at different developmental stages (5, 10, 15, 20, and 25 DPA) of ‘Sumian 20’ (GIF 17 kb)

High Resolution image (TIFF 281 kb)

Fig. S2

Relative expression of heteromeric GhACCase at different seed development stages in two cotton cultivars. The values in Y axis indicate the ratio of the expression of the GhBCCP1, GhBC1, GhCTα2, and GhCTβ to that of GhUBQ7 gene. a-b: Expression of the GhBCCP1, GhBC1, GhCTα2, and GhCTβ genes in seeds of ‘10H1041’; e-h: Expression of the GhBCCP1, GhBC1, GhCTα2, and GhCTβ genes in seeds of ‘Sumian 20’ (GIF 9 kb)

High Resolution image (TIFF 161 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Cui, Y., Liu, Z., Zhao, Y. et al. Overexpression of Heteromeric GhACCase Subunits Enhanced Oil Accumulation in Upland Cotton. Plant Mol Biol Rep 35, 287–297 (2017). https://doi.org/10.1007/s11105-016-1022-y

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11105-016-1022-y

Keywords

Search

Navigation