Skip to main content
SpringerLink
Log in

OsKASI, a β-ketoacyl-[acyl carrier protein] synthase I, is involved in root development in rice (Oryza sativa L.)

  • Original Article
  • Published:
Planta Aims and scope Submit manuscript

Abstract

Main conclusion

The involvement of OsKASI in FA synthesis is found to play a critical role in root development of rice.

The root system plays important roles in plant nutrient and water acquisition. However, mechanisms of root development and molecular regulation in rice are still poorly understood. Here, we characterized a rice (Oryza sativa L.) mutant with shortened roots due to a defect in cell elongation. Map-based cloning revealed that the mutation occurred in a putative 3-oxoacyl-synthase, an ortholog of β-ketoacyl-[acyl carrier protein] synthase I (KASI) in Arabidopsis, thus designated as OsKASI. OsKASI was found to be ubiquitously expressed in various tissues throughout the plant and OsKASI protein was localized in the plastid. In addition, OsKASI deficiency resulted in reduced fertility and a remarkable change in fatty acid (FA) composition and contents in roots and seeds. Our results demonstrate that involvement of OsKASI in FA synthesis is required for root development in rice.

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

Similar content being viewed by others

Abbreviations

ACCase:

Acetyl-CoA carboxylase

ACP:

Malonyl-acyl carrier protein

CoA:

Malonyl-coenzyme A

ENR:

Enoyl-ACP reductase

FA:

Fatty acid

FAS:

Fatty acid synthase

GFP:

Green-fluorescent protein

GUS:

β-Glucuronidase

KAS:

β-Ketoacyl-[acyl carrier protein] synthase

STS:

Sequence-tagged site

VLCFAs:

Very-long-chain fatty acids

WT:

Wild type

References

  • Beemster GT, Fiorani F, Inze D (2003) Cell cycle: the key to plant growth control? Trends Plant Sci 8:154–158

    Article  CAS  PubMed  Google Scholar 

  • Bligh EG, Dyer WJ (1959) A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37:911–917

    Article  CAS  PubMed  Google Scholar 

  • Bonaventure G, Salas JJ, Pollard MR, Ohlrogge JB (2003) Disruption of the FATB gene in Arabidopsis demonstrates an essential role of saturated fatty acids in plant growth. Plant Cell 15:1020–1033

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Chandra-Shekara AC, Venugopal SC, Barman SR, Kachroo A, Kachroo P (2007) Plastidial fatty acid levels regulate resistance gene-dependent defense signaling in Arabidopsis. Proc Natl Acad Sci USA 104:7277–7282

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Chen S, Jin W, Wang M, Zhang F, Zhou J, Jia Q, Wu Y, Liu F, Wu P (2003) Distribution and characterization of over 1000 T-DNA tags in rice genome. Plant J 36:105–113

    Article  CAS  PubMed  Google Scholar 

  • Clough RC, Matthis AL, Barnum SR, Jaworski JG (1992) Purification and characterization of 3-ketoacyl-acyl carrier protein synthase III from spinach. A condensing enzyme utilizing acetyl-coenzyme A to initiate fatty acid synthesis. J Biol Chem 267:20992–20998

    CAS  PubMed  Google Scholar 

  • Galili G (1995) Regulation of lysine and threonine synthesis. Plant Cell 7:899–906

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Gornicki P, Haselkorn R (1993) Wheat acetyl-CoA carboxylase. Plant Mol Biol 22:547–552

    Article  CAS  PubMed  Google Scholar 

  • Guchhait RB, Polakis SE, Dimroth P, Stoll E, Moss J, Lane MD (1974) Acetyl coenzyme A carboxylase system of Escherichia coli. Purification and properties of the biotin carboxylase, carboxyltransferase, and carboxyl carrier protein components. J Biol Chem 249:6633–6645

    CAS  PubMed  Google Scholar 

  • Harwood JL (1988) Fatty acid metabolism. Annu Rev Plant Physiol Plant Mol Biol 39:101–138

    Article  CAS  Google Scholar 

  • Inukai Y, Sakamoto T, Morinaka Y, Miwa M, Kojima M, Tanimoto E, Yamamoto H, Sato K, Katayama Y, Matsuoka M (2012) ROOT GROWTH INHIBITING, a rice endo-1, 4-β-D-glucanase, regulates cell wall loosening and is essential for root elongation. J Plant Growth Regul 31:373–381

    Article  CAS  Google Scholar 

  • Jackowski S, Rock CO (1987) Acetoacetyl-acyl carrier protein synthase, a potential regulator of fatty acid biosynthesis in bacteria. J Biol Chem 262:7927–7931

    CAS  PubMed  Google Scholar 

  • Jefferson RA, Kavanagh TA, Bevan MW (1987) GUS fusions: beta-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J 6:3901

    CAS  PubMed Central  PubMed  Google Scholar 

  • Jia L, Zhang B, Mao C, Li J, Wu Y, Wu P, Wu Z (2008) OsCYT-INV1 for alkaline/neutral invertase is involved in root cell development and reproductivity in rice (Oryza sativa L.). Planta 228:51–59

    Article  CAS  PubMed  Google Scholar 

  • Jia L, Wu Z, Hao X, Carrie C, Zheng L, Whelan J, Wu Y, Wang S, Wu P, Mao C (2011) Identification of a novel mitochondrial protein, short postembryonic roots 1 (SPR1), involved in root development and iron homeostasis in Oryza sativa. New Phytol 189:843–855

    Article  CAS  PubMed  Google Scholar 

  • Jiang H, Wang S, Dang L, Wang S, Chen H, Wu Y, Jiang X, Wu P (2005) A novel short-root gene encodes a glucosamine-6-phosphate acetyltransferase required for maintaining normal root cell shape in rice. Plant Physiol 138:232–242

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Jiang CJ, Shimono M, Maeda S, Inoue H, Mori M, Hasegawa M, Sugano S, Takatsuji H (2009) Suppression of the rice fatty-acid desaturase gene OsSSI2 enhances resistance to blast and leaf blight diseases in rice. Mol Plant Microbe Interact 22:820–829

    Article  CAS  PubMed  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 

  • Kachroo P, Shanklin J, Shah J, Whittle EJ, Klessig DF (2001) A fatty acid desaturase modulates the activation of defense signaling pathways in plants. Proc Natl Acad Sci USA 98:9448–9453

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Kachroo A, Shanklin J, Whittle E, Lapchyk L, Hildebrand D, Kachroo P (2007) The Arabidopsis stearoyl-acyl carrier protein-desaturase family and the contribution of leaf isoforms to oleic acid synthesis. Plant Mol Biol 63:257–271

    Article  CAS  PubMed  Google Scholar 

  • Kachroo A, Fu DQ, Havens W, Navarre D, Kachroo P, Ghabrial SA (2008) An oleic acid-mediated pathway induces constitutive defense signaling and enhanced resistance to multiple pathogens in soybean. Mol Plant Microbe Interact 21:564–575

    Article  CAS  PubMed  Google Scholar 

  • Kashiwagi J, Iwama K, Hasegawa T (2000) Stability of phenotypic variation of root length over environmental conditions in the seedling generation of potato. Jpn J Crop Sci 69:332–336

    Article  Google Scholar 

  • Kim CM, Park SH, Je BI, Park SH, Park SJ, Piao HL, Eun MY, Dolan L, Han C-D (2007) OsCSLD1, a cellulose synthase-like D1 gene, is required for root hair morphogenesis in rice. Plant Physiol 143:1220–1230

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Li J, Zhu S, Song X, Shen Y, Chen H, Yu J, Yi K, Liu Y, Karplus VJ, Wu P, Deng XW (2006) A rice glutamate receptor–like gene is critical for the division and survival of individual cells in the root apical meristem. Plant Cell 18:340–349

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Li M, Xiong G, Li R, Cui J, Tang D, Zhang B, Pauly M, Cheng Z, Zhou Y (2009) Rice cellulose synthase-like D4 is essential for normal cell-wall biosynthesis and plant growth. Plant J 60:1055–1069

    Article  CAS  PubMed  Google Scholar 

  • Lynen F (1980) On the structure of fatty acid synthetase of yeast. Eur J Biochem 112:431–442

    Article  CAS  PubMed  Google Scholar 

  • Ma N, Wang Y, Qiu S, Kang Z, Che S, Wang G, Huang J (2013) Overexpression of OsEXPA8, a root-specific gene, improves rice growth and root system architecture by facilitating cell extension. PLoS One 8:e75997

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Metcalfe LD, Schmitz AA, Pelka JR (1966) Rapid preparation of fatty acid esters from lipids for gas chromatographic analysis. Anal Chem 38:514–515

    Article  CAS  Google Scholar 

  • Mou Z, He Y, Dai Y, Liu X, Li J (2000) Deficiency in fatty acid synthase leads to premature cell death and dramatic alterations in plant morphology. Plant Cell 12:405–418

    Article  CAS  PubMed Central  PubMed  Google Scholar 

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

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Qin YM, Hu CY, Pang Y, Kastaniotis AJ, Hiltunen JK, Zhu YX (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 Central  PubMed  Google Scholar 

  • Qin C, Li Y, Gan J, Wang W, Zhang H, Liu Y, Wu P (2013) OsDGL1, a homolog of an oligosaccharyltransferase complex subunit, is involved in N-glycosylation and root development in rice. Plant Cell Physiol 54:129–137

    Article  CAS  PubMed  Google Scholar 

  • Rebouillat J, Dievart A, Verdeil J, Escoute J, Giese G, Breitler J, Gantet P, Espeout S, Guiderdoni E, Périn C (2009) Molecular genetics of rice root development. Rice 2:15–34

    Article  Google Scholar 

  • Roudier F, Gissot L, Beaudoin F, Haslam R, Michaelson L, Marion J, Molino D, Lima A, Bach L, Morin H, Tellier F, Palauqui JC, Bellec Y, Renne C, Miquel M, Dacosta M, Vignard J, Rochat C, Markham JE, Moreau P, Napier J, Faure JD (2010) Very-long-chain fatty acids are involved in polar auxin transport and developmental patterning in Arabidopsis. Plant Cell 22:364–375

    Article  CAS  PubMed Central  PubMed  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 

  • Shah J, Kachroo P, Nandi A, Klessig DF (2001) A recessive mutation in the Arabidopsis SSI2 gene confers SA-and NPR1-independent expression of PR genes and resistance against bacterial and oomycete pathogens. Plant J 25:563–574

    Article  CAS  PubMed  Google Scholar 

  • Shelley IJ, Nishiuchi S, Shibata K, Inukai Y (2013) SLL1, which encodes a member of the stearoyl-acyl carrier protein fatty acid desaturase family, is involved in cell elongation in lateral roots via regulation of fatty acid content in rice. Plant Sci 207:12–17

    Article  CAS  PubMed  Google Scholar 

  • Shimakata T, Stumpf PK (1982) Purification and characterizations of β-Ketoacyl-[acyl-carrier-protein] reductase, β-hydroxyacyl-[acyl-carrier-protein] dehydrase, and enoyl-[acyl-carrier-protein] reductase from Spinacia oleracea leaves. Arch Biochem Biophys 218:77–91

    Article  CAS  PubMed  Google Scholar 

  • Smith S (1994) The animal fatty acid synthase: one gene, one polypeptide, seven enzymes. FASEB J 8:1248–1259

    CAS  PubMed  Google Scholar 

  • Teo YH, Beyrouty CA, Norman RJ, Gbur EE (1995) Nutrient uptake relationship to root characteristics of rice. Plant Soil 171:297–302

    Article  CAS  Google Scholar 

  • Wakil SJ (1989) Fatty acid synthase, a proficient multifunctional enzyme. Biochemistry 28:4523–4530

    Article  CAS  PubMed  Google Scholar 

  • Wang S, Xu Y, Li Z, Zhang S, Lim JM, Lee KO, Li C, Qian Q, de Jiang A, Qi Y (2014) OsMOGS is required for N-glycan formation and auxin-mediated root development in rice (Oryza sativa L.). Plant J 78:632–645

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Wei Q, Li J, Zhang L, Wu P, Chen Y, Li M, Jiang H, Wu G (2012) Cloning and characterization of a β-ketoacyl-acyl carrier protein synthase II from Jatropha curcas. J Plant Physiol 169:816–824

    Article  CAS  PubMed  Google Scholar 

  • Wu GZ, Xue HW (2010) Arabidopsis β-ketoacyl-[acyl carrier protein] synthase I is crucial for fatty acid synthesis and plays a role in chloroplast division and embryo development. Plant Cell 22:3726–3744

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Xia J, Yamaji N, Che J, Shen RF, Ma JF (2014) Normal root elongation requires arginine produced by argininosuccinate lyase in rice. Plant J 78:215–226

    Article  CAS  PubMed  Google Scholar 

  • Yamauchi A, Pardales JR, Kono Y (1996) Root system structure and its relation to stress tolerance. In: Ito O, Johansen C, Gyamfi JJA, Katayama KK, Kumar JVDK, Rao TJR (eds) Dynamics of roots and nitrogen in cropping systems of the semi-arid tropics. JIRCAS, Tsukuba, pp 211–233

    Google Scholar 

  • Yasuno R, von Wettstein-Knowles P, Wada H (2004) Identification and molecular characterization of the β-ketoacyl-[acyl carrier protein] synthase component of the Arabidopsis mitochondrial fatty acid synthase. J Biol Chem 279:8242–8251

    Article  CAS  PubMed  Google Scholar 

  • Yoshida S, Forno DA, Cock JH, Gomez KA (1976) Routine procedure for growing rice plants in culture solution. Laboratory manual for physiological studies of rice. IRRI, Los Banos, pp 61–66

    Google Scholar 

  • Zhang JW, Xu L, Wu YR, Chen XA, Liu Y, Zhu SH, Ding WN, Wu P, Yi KK (2012) OsGLU3, a putative membrane-bound endo-1,4-beta-glucanase, is required for root cell elongation and division in rice (Oryza sativa L.). Mol Plant 5:176–186

    Article  PubMed  Google Scholar 

  • 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 17:1467–1481

    Article  CAS  PubMed Central  PubMed  Google Scholar 

Download references

Acknowledgments

We are grateful to Prof. Ping Wu (College of Life Science, Zhejiang University, Hangzhou, China) for providing the mutant. This research was supported by the National Natural Science Foundation of China [grant numbers 31371595, 31300246 and 31071388] and Hulan’s Excellent Doctor Foundation of Ningbo University, China.

Conflict of interest

The authors declare that they have no conflict of interest.

Author information

Author notes

    Authors and Affiliations

    1. College of Science and Technology, Ningbo University, Ningbo, 315211, People’s Republic of China

      Wona Ding, Zhichong Pan & Shihua Zhu

    2. School of Marine Sciences, Ningbo University, Ningbo, 315211, People’s Republic of China

      Li Lin, Xianbo Xiang & Jing Wu

    3. Department of Botany, La Trobe University, Melbourne, VIC, Australia

      Botao Zhang

    Authors
    1. Wona Ding
      View author publications

      You can also search for this author in PubMed Google Scholar

    2. Li Lin
      View author publications

      You can also search for this author in PubMed Google Scholar

    3. Botao Zhang
      View author publications

      You can also search for this author in PubMed Google Scholar

    4. Xianbo Xiang
      View author publications

      You can also search for this author in PubMed Google Scholar

    5. Jing Wu
      View author publications

      You can also search for this author in PubMed Google Scholar

    6. Zhichong Pan
      View author publications

      You can also search for this author in PubMed Google Scholar

    7. Shihua Zhu
      View author publications

      You can also search for this author in PubMed Google Scholar

    Corresponding author

    Correspondence to Shihua Zhu.

    Additional information

    W. Ding and L. Lin contributed equally to this work.

    Electronic supplementary material

    Below is the link to the electronic supplementary material.

    Supplementary material 1 (PDF 5862 kb)

    Rights and permissions

    Reprints and permissions

    About this article

    Check for updates. Verify currency and authenticity via CrossMark

    Cite this article

    Ding, W., Lin, L., Zhang, B. et al. OsKASI, a β-ketoacyl-[acyl carrier protein] synthase I, is involved in root development in rice (Oryza sativa L.). Planta 242, 203–213 (2015). https://doi.org/10.1007/s00425-015-2296-2

    Download citation

    • Received:

    • Accepted:

    • Published:

    • Issue Date:

    • DOI: https://doi.org/10.1007/s00425-015-2296-2

    Keywords

    Search

    Navigation