Skip to main content
Log in

Overexpression of ShCHL P in tomato improves seedling growth and increases tolerance to salt, osmotic, and oxidative stresses

  • Original paper
  • Published:
Plant Growth Regulation Aims and scope Submit manuscript

Abstract

Geranylgeranyl reductase (CHL P) catalyzes the reduction of geranylgeranyl diphosphate to phytyl diphosphate and provides phytol for both chlorophyll (Chl) and tocopherol (TP) synthesis. Our previous study has found that the Solanum habrochaites CHL P (ShCHL P) gene was repressed by cold stress. In this study, we functionally characterized this gene with respect to abiotic stress tolerance. ShCHL P is expressed highly in leaves and stems, and barely in roots. Also, its expression was suppressed by low and high temperatures, drought, salt, and oxidative stresses. Transgenic tomato plants overexpressing ShCHL P showed increased levels of Chl and α-TP in leaves. In contrast, Chl and α-TP contents were reduced in the co-suppression plants, which exhibited chlorosis. These results confirmed the previous findings that CHL P is essential for Chl and TP synthesis in plants. Moreover, the ShCHL P overexpression and suppression lines showed improved and inhibited early seedling growth under normal, salt, and osmotic stress conditions, respectively, as compared with the wild type. Surprisingly, both overexpression and suppression of CHL P in transgenic tomato enhanced tolerance to methyl viologen-induced oxidative stress. These results indicate that tomato CHL P plays an important role in response to abiotic stress through regulation of Chl and TP synthesis. CHL P might be a good candidate gene for genetic improvement of plant growth under abiotic stress conditions in tomato.

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

Access this article

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Abbreviations

Chl:

Chlorophyll

CHL P:

Geranylgeranyl reductase

GGPP:

Geranylgeranyl diphosphate

PhyPP:

Phytyl diphosphate

qRT-PCR:

Quantitative real-time PCR

ROS:

Reactive oxygen species

TP:

Tocopherol

MV:

Methyl viologen

WT:

Wild type

References

  • Abbasi AR, Hajirezaei M, Hofius D, Sonnewald U, Voll LM (2007) Specific roles of alpha- and gamma-tocopherol in abiotic stress responses of transgenic tobacco. Plant Physiol 143:1720–1738

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Almeida J, Quadrana L, Asis R, Setta N, de Godoy F, Bermudez L, Otaiza SN, Correa da Silva JV, Fernie AR, Carrari F, Rossi M (2011) Genetic dissection of vitamin E biosynthesis in tomato. J Exp Bot 62:3781–3798

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373–399

    Article  CAS  PubMed  Google Scholar 

  • Bollivar DW, Wang S, Allen JP, Bauer CE (1994) Molecular genetic analysis of terminal steps in bacteriochlorophyll a biosynthesis: characterization of a Rhodobacter capsulatus strain that synthesizes geranylgeraniol-esterified bacteriochlorophyll a. Biochemistry 33:12763–12768

    Article  CAS  PubMed  Google Scholar 

  • Brigelius-Flohe R, Traber MG (1999) Vitamin E: function and metabolism. FASEB J 13:1145–1155

    CAS  PubMed  Google Scholar 

  • Bruno L, Chiappetta A, Muzzalupo I, Gagliardi C, Iaria D, Bruno A, Greco M, Giannino D, Perri E, Bitonti MB (2009) Role of geranylgeranyl reductase gene in organ development and stress response in olive (Olea europaea) plants. Funct Plant Biol 36:370–381

    Article  CAS  Google Scholar 

  • Cahoon EB, Hall SE, Ripp KG, Ganzke TS, Hitz WD, Coughlan SJ (2003) Metabolic redesign of vitamin E biosynthesis in plants for tocotrienol production and increased antioxidant content. Nat Biotechnol 21:1082–1087

    Article  CAS  PubMed  Google Scholar 

  • Cogoni C, Macino G (1999) Homology-dependent gene silencing in plants and fungi: a number of variations on the same theme. Curr Opin Microbiol 2:657–662

    Article  CAS  PubMed  Google Scholar 

  • Dalal VK, Tripathy BC (2012) Modulation of chlorophyll biosynthesis by water stress in rice seedlings during chloroplast biogenesis. Plant Cell Environ 35:1685–1703

    Article  CAS  PubMed  Google Scholar 

  • Dinakar C, Abhaypratap V, Yearla SR, Raghavendra AS, Padmasree K (2010) Importance of ROS and antioxidant system during the beneficial interactions of mitochondrial metabolism with photosynthetic carbon assimilation. Planta 231:461–474

    Article  CAS  PubMed  Google Scholar 

  • Emanuelsson O, Nielsen H, von Heijne G (1999) ChloroP, a neural network-based method for predicting chloroplast transit peptides and their cleavage sites. Protein Sci 8:978–984

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Espinoza A, San Martin A, Lopez-Climent M, Ruiz-Lara S, Gomez-Cadenas A, Casaretto JA (2013) Engineered drought-induced biosynthesis of alpha-tocopherol alleviates stress-induced leaf damage in tobacco. J Plant Physiol 170:1285–1294

    Article  CAS  PubMed  Google Scholar 

  • Falk J, Munne-Bosch S (2010) Tocochromanol functions in plants: antioxidation and beyond. J Exp Bot 61:1549–1566

    Article  CAS  PubMed  Google Scholar 

  • Fromme P, Melkozernov A, Jordan P, Krauss N (2003) Structure and function of photosystem I: interaction with its soluble electron carriers and external antenna systems. FEBS Lett 555:40–44

    Article  CAS  PubMed  Google Scholar 

  • Giannino D, Condello E, Bruno L, Testone G, Tartarini A, Cozza R, Innocenti AM, Bitonti MB, Mariotti D (2004) The gene geranylgeranyl reductase of peach (Prunus persica [L.] Batsch) is regulated during leaf development and responds differentially to distinct stress factors. J Exp Bot 55:2063–2073

    Article  CAS  PubMed  Google Scholar 

  • Grasses T, Grimm B, Koroleva O, Jahns P (2001) Loss of alpha-tocopherol in tobacco plants with decreased geranylgeranyl reductase activity does not modify photosynthesis in optimal growth conditions but increases sensitivity to high-light stress. Planta 213:620–628

    Article  CAS  PubMed  Google Scholar 

  • Havaux M, Lutz C, Grimm B (2003) Chloroplast membrane photostability in chlP transgenic tobacco plants deficient in tocopherols. Plant Physiol 132:300–310

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hussain N, Irshad F, Jabeen Z, Shamsi IH, Li Z, Jiang L (2013) Biosynthesis, structural, and functional attributes of tocopherols in planta; past, present, and future perspectives. J Agric Food Chem 61:6137–6149

    Article  CAS  PubMed  Google Scholar 

  • Keegstra K, Cline K (1999) Protein import and routing systems of chloroplasts. Plant Cell 11:557–570

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Keller Y, Bouvier F, d’Harlingue A, Camara B (1998) Metabolic compartmentation of plastid prenyllipid biosynthesis—Evidence for the involvement of a multifunctional geranylgeranyl reductase. Eur J Biochem 251:413–417

    Article  CAS  PubMed  Google Scholar 

  • Ketting RF, Plasterk RH (2000) A genetic link between co-suppression and RNA interference in C. elegans. Nature 404:296–298

    Article  CAS  PubMed  Google Scholar 

  • Kumar D, Yusuf MA, Singh P, Sardar M, Sarin NB (2013) Modulation of antioxidant machinery in alpha-tocopherol-enriched transgenic Brassica juncea plants tolerant to abiotic stress conditions. Protoplasma 250:1079–1089

    Article  CAS  PubMed  Google Scholar 

  • Liu X, Hua X, Guo J, Qi D, Wang L, Liu Z, Jin Z, Chen S, Liu G (2008) Enhanced tolerance to drought stress in transgenic tobacco plants overexpressing VTE1 for increased tocopherol production from Arabidopsis thaliana. Biotechnol Lett 30:1275–1280

    Article  CAS  PubMed  Google Scholar 

  • Liu H, Ouyang B, Zhang J, Wang T, Li H, Zhang Y, Yu C, Ye Z (2012) Differential modulation of photosynthesis, signaling, and transcriptional regulation between tolerant and sensitive tomato genotypes under cold stress. PLoS One 7:e50785

    Article  PubMed Central  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Lovdal T, Lillo C (2009) Reference gene selection for quantitative real-time PCR normalization in tomato subjected to nitrogen, cold, and light stress. Anal Biochem 387:238–242

    Article  CAS  PubMed  Google Scholar 

  • Matringe M, Ksas B, Rey P, Havaux M (2008) Tocotrienols, the unsaturated forms of vitamin E, can function as antioxidants and lipid protectors in tobacco leaves. Plant Physiol 147:764–778

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Mittler R, Vanderauwera S, Suzuki N, Miller G, Tognetti VB, Vandepoele K, Gollery M, Shulaev V, Van Breusegem F (2011) ROS signaling: the new wave? Trends Plant Sci 16:300–309

    Article  CAS  PubMed  Google Scholar 

  • Mohanty S, Grimm B, Tripathy BC (2006) Light and dark modulation of chlorophyll biosynthetic genes in response to temperature. Planta 224:692–699

    Article  CAS  PubMed  Google Scholar 

  • Munne-Bosch S (2005) Linking tocopherols with cellular signaling in plants. New Phytol 166:363–366

    Article  CAS  PubMed  Google Scholar 

  • Ouyang B, Chen YH, Li HX, Qian CJ, Huang SL, Ye ZB (2005) Transformation of tomatoes with osmotin and chitinase genes and their resistance to Fusarium wilt. J Hortic Sci Biotechnol 80:517–522

    CAS  Google Scholar 

  • Park MR, Cho EA, Rehman S, Yun SJ (2010) Expression of a sesame geranylgeranyl reductase cDNA is induced by light but repressed by abscisic acid and ethylene. Pak J Bot 42:1815–1825

    CAS  Google Scholar 

  • Pino LE, Lombardi-Crestana S, Azevedo MS, Scotton DC, Borgo L, Quecini V, Figueira A, Peres LE (2010) The Rg1 allele as a valuable tool for genetic transformation of the tomato ‘Micro-Tom’ model system. Plant Methods 6:23

    Article  PubMed Central  PubMed  Google Scholar 

  • Quadrana L, Almeida J, Otaiza SN, Duffy T, Correa da Silva JV, de Godoy F, Asis R, Bermudez L, Fernie AR, Carrari F, Rossi M (2013) Transcriptional regulation of tocopherol biosynthesis in tomato. Plant Mol Biol 81:309–325

    Article  CAS  PubMed  Google Scholar 

  • Soll J, Kemmerling M, Schultz G (1980) Tocopherol and plastoquinone synthesis in spinach chloroplasts subfractions. Arch Biochem Biophys 204:544–550

    Article  CAS  PubMed  Google Scholar 

  • Soll J, Schultz G, Rudiger W, Benz J (1983) Hydrogenation of geranylgeraniol: two pathways exist in spinach chloroplasts. Plant Physiol 71:849–854

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Suzuki N, Miller G, Morales J, Shulaev V, Torres MA, Mittler R (2011) Respiratory burst oxidases: the engines of ROS signaling. Curr Opin Plant Biol 14:691–699

    Article  CAS  PubMed  Google Scholar 

  • Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599

    Article  CAS  PubMed  Google Scholar 

  • Tanaka R, Oster U, Kruse E, Rudiger W, Grimm B (1999) Reduced activity of geranylgeranyl reductase leads to loss of chlorophyll and tocopherol and to partially geranylgeranylated chlorophyll in transgenic tobacco plants expressing antisense RNA for geranylgeranyl reductase. Plant Physiol 120:695–704

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Wang P, Li C, Wang Y, Huang R, Sun C, Xu Z, Zhu J, Gao X, Deng X (2014) Identification of a geranylgeranyl reductase gene for chlorophyll synthesis in rice. Springerplus 3:201

    Article  PubMed Central  PubMed  Google Scholar 

  • Yusuf MA, Kumar D, Rajwanshi R, Strasser RJ, Tsimilli-Michael M, Govindjee Sarin NB (2010) Overexpression of gamma-tocopherol methyl transferase gene in transgenic Brassica juncea plants alleviates abiotic stress: physiological and chlorophyll a fluorescence measurements. Biochim Biophys Acta 1797:1428–1438

    Article  CAS  PubMed  Google Scholar 

  • Zhan GM, Li RJ, Hu ZY, Liu J, Deng LB, Lu SY, Hua W (2014) Co-suppression of RBCS3B in Arabidopsis leads to severe photoinhibition caused by ROS accumulation. Plant Cell Rep 33:1091–1108

    Article  CAS  PubMed  Google Scholar 

  • Zhang J, Kirkham MB (1996) Antioxidant responses to drought in sunflower and sorghum seedlings. New Phytol 132:361–373

    Article  CAS  Google Scholar 

  • Zhang H, Mao X, Wang C, Jing R (2010) Overexpression of a common wheat gene TaSnRK2.8 enhances tolerance to drought, salt and low temperature in Arabidopsis. PLoS One 5:e16041

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Zhou Y, Gong Z, Yang Z, Yuan Y, Zhu J, Wang M, Yuan F, Wu S, Wang Z, Yi C, Xu T, Ryom M, Gu M, Liang G (2013) Mutation of the light-induced yellow leaf 1 gene, which encodes a geranylgeranyl reductase, affects chlorophyll biosynthesis and light sensitivity in rice. PLoS One 8:e75299

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ziaf K, Loukehaich R, Gong P, Liu H, Han Q, Wang T, Li H, Ye Z (2011) A multiple stress-responsive gene ERD15 from Solanum pennellii confers stress tolerance in tobacco. Plant Cell Physiol 52:1055–1067

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by the National Natural Science Foundation of China (Grant No. 31301789). We would like to thank Dr. Zhibiao Ye (Huazhong Agricultural University) for reading the manuscript and making helpful suggestions.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Hui Liu.

Electronic supplementary material

Supplementary Fig. 1 Alignment and phylogenetic relationship of ShCHL P with other CHL Ps. a Alignment of ShCHL P with CHL Ps from other plant species: SlCHL P (XP_004235993), NtCHL P (Q9ZS34) and AtCHL P (NP_177587). The black arrow indicates the editing site for the transit peptide. Asterisks indicate the conserved NADPH-binding motif (GXGXXG). b The phylogenetic relationship among CHL Ps. Accession numbers for other CHL P proteins are as follows: S. habrochaites (KM226160), S. tuberosum (XP_006364592), Sesamum indicum (ADK35887), Vitis vinifera (XP_002284906), Olea europaea (ABD73016), Glycine max (AAD28640), Medicago truncatula (AAX63898), Populus trichocarpa (XP_002317979), Hevea brasiliensis (BAH10639), Prunus persica (AAP55675), Oryza sativa (AGX32158), Paulinella chromatophora (YP_002048921).

Supplementary material 1 (TIFF 3806 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Liu, H., Liu, J., Zhao, MM. et al. Overexpression of ShCHL P in tomato improves seedling growth and increases tolerance to salt, osmotic, and oxidative stresses. Plant Growth Regul 77, 211–221 (2015). https://doi.org/10.1007/s10725-015-0054-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10725-015-0054-x

Keywords

Navigation