Skip to main content
SpringerLink
Log in

Integrating transcriptome and target metabolome variability in doubled haploids of Allium cepa for abiotic stress protection

  • Published:
Molecular Breeding Aims and scope Submit manuscript

Abstract

Environmental stress conditions such as drought, heat, salinity, or pathogen infection can have a devastating impact on plant growth and yield, resulting in a need for stress-tolerant crop varieties. Crossbreeding tropical and cultivated onion species produced a hybrid F1 generation possessing genetic and metabolic parental properties that aided abiotic stress tolerance. Targeted metabolite profiling using liquid chromatography–tandem mass spectrometry integrated with transcriptional analysis of their relevant genes provided insights into the metabolic and genomic architecture of the onion doubled haploid (Allium cepa L., DHC), shallot doubled haploid (A. cepa L. Aggregatum group, DHA), and F1 hybrid. Out of a complete set of 113 targeted metabolites, 49 metabolites were found to be statistically significantly different between genotypes: 11 metabolites were characteristic for DHC, 10 for DHA, 14 for F1, and 14 metabolites were shared among the three genotypes. Several key genes and metabolites introgressed in abiotic stress response were up-regulated in DHA and F1 genotypes as compared to DHC. Principal component analysis and Volcano plot analysis revealed that metabolic traits and their relevant genes (namely, amino acid, carbohydrate, flavonoid, and phospholipid biosynthesis) were strongly linked with DHA and F1, reflecting the adaptability of DHA and F1 toward abiotic stress as compared to DHC.

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

References

  • Alan AR, Mutschler MA, Brant A, Cobb E, Earle ED (2003) Production of gynogenic plants from hybrids of Allium cepa L. and A. roylei Stearn. Plant Sci 165:1201–1211

    Article  CAS  Google Scholar 

  • Alcàzar R, Altabella T, Marco F, Bortolotti C, Reymond M, Koncz C, Carrasco P, Tiburico AF (2010) Polyamines: molecules with regulatory functions in plant abiotic stress tolerance. Planta 231:1237–1249

    Article  PubMed  Google Scholar 

  • Atkinson NJ, Urwin PE (2012) The interaction of plant biotic and abiotic stresses: from genes to the field. J Exp Bot 63:3523–3543

    Article  CAS  PubMed  Google Scholar 

  • Basu PS, Sharma A, Garg ID, Sukumaran NP (1999) Tuber sink modifies photosynthetic response in potato under water stress. Environ Exp Bot 42:25–39

    Article  Google Scholar 

  • Berglund T (1994) Nicotinamide, a missing link in the early stress response in eukaryotic cells-a hypothesis with special reference to oxidative stress in plants. FEBS Lett 351:145–159

    Article  CAS  PubMed  Google Scholar 

  • Brouwer C, Prins K, Heibloem M (1989) Irrigation water management: irrigation scheduling. FAO, Training manual No. 4. ftp://ftp.fao.org/agl/aglw/fwm/Manual4.pdf

  • Burget EG, Verma R, Molhoj M, Reiter WD (2003) The biosynthesis of L-arabinose in plans: molecular cloning and characterization of a Golgi-localized UDP-D-xylose 4-epimerase encoded by the MUR4 gene of Arabidopsis. Plant Cell 15:523–531

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Curien G, Dumas R, Ravanel S, Douce R (1996) Characterization of an Arabidopsis thaliana cDNA encoding an S-adenosylmethionine-sensitive threonine synthase. Threonine synthase from higher plants. FEBS Lett 390:85–90

    Article  CAS  PubMed  Google Scholar 

  • Currah L (2002) Onions in the tropics: cultivars and country reports. In: Rabinowitch HD, Currah L (eds) Allium crop science: recent advances. CABI Publishing, Wallingford, pp 379–407

    Chapter  Google Scholar 

  • Dancs G, Kondark M, Banfalvi Z (2008) The effects of enhanced methionine synthesis on amino acid and anthocyanin content of potato tubers. BMC Plant Biol 65:1–10

    Google Scholar 

  • Dauwe R, Holliday JA, Aitken SN, Mansfield SD (2012) Metabolic dynamics during autumn cold acclimation within and among populations of Sitka spruce (Picea sitchensis). New Phytol 194:192–205

    Article  CAS  PubMed  Google Scholar 

  • Evers D, lef′evre I, Legay S, Lamoureux D, Hausman JF, Rosales ROG, Marca LRT, Hoffmann L, Bonierbale M, Schafleitner R (2010) Identification of drought-responsive compounds in potato through a combined transcriptomic and targeted metabolite approach. J Exp Bot 61:2327–2343

    Article  CAS  PubMed  Google Scholar 

  • Ghanda B, Xia Y, Mandal MK, Yu K, Sekine KT, Gao QM, Selote D, Hu Y, Stromberg A, Navarre D, Kachroo A, Kachroo P (2011) Glycerol-3-phosphate is a critical mobile inducer of systemic immunity in plants. Nat Genet 43:421–427

    Article  Google Scholar 

  • Gupta AK, Kaur N (2005) Sugar signaling and gene expression in relation to carbohydrate metabolism under abiotic stresses in plants. J Biosci 30:761–776

    Article  CAS  PubMed  Google Scholar 

  • Hacham Y, Matityahu I, Schuster G, Amir R (2008) Overexpression of mutated forms of aspartate kinase and cystathionine γ-synthase in tobacco leaves resulted in the high accumulation of methionine and threonine. Plant J 54:260–271

    Article  CAS  PubMed  Google Scholar 

  • Hoa QV, El-Sayed MA, Ito SI, Yamauchi N, Shigyo M (2012) Discovery of a new source of resistance to Fusarium oxysporum, cause of Fusarium wilt in Allium fistulosum, located on chromosome 2 of Allium cepa Aggregatum group. Genome 55:797–807

    Article  Google Scholar 

  • Joshi V, Joung JG, Fei Z, Jander G (2010) Interdependence of threonine, methionine and isoleucine metabolism in plants: accumulation and transcriptional regulation under abiotic stress. Amino Acids 39:933–947

    Article  CAS  PubMed  Google Scholar 

  • Keunen E, Peshev D, Vangronsveld J, Van den Ende W, Cuypers A (2013) Plant sugars are crucial players in the oxidative challenge during abiotic stress: extending the traditional concept. Plant Cell Environ 36:1242–1255

    Article  CAS  PubMed  Google Scholar 

  • Lehle L, Tanner W (1973) The function of myo-inositol in the biosynthesis of raffinose. Eur J Biochem 38:103–110

    Article  CAS  PubMed  Google Scholar 

  • Lima RB, Santos TBD, Vieira LGE, Ferrarese MDLL, Ferrarese-Filho O, Donatti L, Boeger MRT, Petkowicz CLDO (2013) Heat stress causes alterations in the cell-wall polymers and anatomy of coffee leaves (Coffea arabica L.). Carbohydr Poly 93:135–143

    Article  CAS  Google Scholar 

  • Liu HL, Dai XY, Xu YY, Chong K (2007) Over-expression of OsUGE-1 altered raffinose level and tolerance to abiotic stress but not morphology in Arabidopsis. J Plant Physiol 164:1384–1390

    Article  CAS  PubMed  Google Scholar 

  • Masamura N, Yaguchi S, Ono Y, Nakajima T, Masuzaki SI, Imai S, Yamauchi N, Shigyo M (2011) Characterization of amino acid and S-alk(en)yl-l-cysteine sulfoxide production in Japanese bunching onion carrying extra chromosome of shallot. J Japan Soc Hort Sci 80:322–333

    Article  CAS  Google Scholar 

  • Masuzaki S, Shigyo M, Yamaguchi N (2006) Direct comparison between genomic constitution and flavonoid contents in Allium multiple alien addition lines reveals chromosomal locations of genes related to biosynthesis from dihydrokaempferol to quercetin glucosides in scaly leaf of shallot (Allium cepa L.). Theor Appl Gen 12:607–617

    Article  Google Scholar 

  • Minorsky PV (2002) Trigonelline: a diverse regulator in plants. Plant Physiol 128:7–8

    Article  PubMed Central  CAS  Google Scholar 

  • Mitsuda N, Ohme-Takagi M (2009) Functional analysis of transcription factors in Arabidopsis. Plant Cell Physiol 50:123–1248

    Article  Google Scholar 

  • Moore JP, Nguema-Ona E, Chevalier L, Lindsey GC, Brandt WE, Lerouge P, Farrant JM, Driouich A (2006) Response of the leaf cell wall to desiccation in the resurrection plant Myrothamnus flabellifolius. Plant Physiol 141:651–662

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Newton AC, Johnson SN, Gregory PJ (2011) Implications of climate change for diseases, crop yields and food security. Euphytica 179:3–18

    Article  Google Scholar 

  • Nishizawa A, Yabuta Y, Yoshida E, Maruta T, Yoshimura K, Shigeoka S (2006) Arabidopsis heat shock transcription factors A2 as a key regulator in response to several types of environmental stress. Plant J 48:535–547

    Article  CAS  PubMed  Google Scholar 

  • Nuccio ML, Rhodes D, McNeil SD, Hanson AD (1999) Metabolic engineering of plants for osmotic stress resistance. Curr Opin Plant Biol 2:128–134

    Article  CAS  PubMed  Google Scholar 

  • Parker D, Beckmann M, Zubair H, Enot DP, Rios ZC, Overy DP, Snowdon S, Talbot NJ, Draper J (2009) Metabolomic analysis reveals a common pattern of metabolic re-programming during invasion of three host plant species by Magnaporthe grisea. Plant J 59:723–737

    Article  CAS  PubMed  Google Scholar 

  • Peremarti A, Mare C, Aprile A, Roncaglia E, Cattivelli L, Villegas D, Royo C (2014) Transcriptomic and proteomic analyses of a pale-green durum wheat mutant shows variations in photosystem components and metabolic deficiencies under drought stress. BMC Genomics 15:125–152

    Article  PubMed Central  PubMed  Google Scholar 

  • Peshev D, Van den Ende W (2013) Sugars as antioxidants in plants. In: Tuteja N, Gill S (eds) Crop improvement under adverse conditions. Springer, Berlin, pp 285–308

    Google Scholar 

  • Peters S, Mundree SG, Thomson JA, Farrant JM, Keller F (2007) Protection mechanism in the resurrection plant Xerophytaviscosa (Baker): both sucrose and raffinose family oligosaccharides (ROFs) accumulate in leaves in response to water deficit. J Exp Bot 58:1947–1956

    Article  CAS  PubMed  Google Scholar 

  • Robinson A, Ukrainetz NK, Kang KY, Mansfield SD (2007) Metabolite profiling of Douglas-fir (Pseudotsugamenziesii) field trails reveals strong environmental and weak genetic variation. New Phytol 147:762–773

    Article  Google Scholar 

  • Rumpho ME, Edwards GE, Loescher WH (1983) A pathway for photosynthetic carbon flow to mannitol in celery leaves. Activity and localization of key enzymes (Apium graveolens). Plant Physiol 73:869–873

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Saito K, Matsuda F (2010) Metabolomics for functional genomics, system biology, and biotechnology. Plant Biol 61:463–489

    Article  CAS  Google Scholar 

  • Saravitz DM, Pharr DM, Carter TE (1987) Galactinol synthase activity and soluble sugars in developing seeds of four soybean genotypes. Plant Physiol 83:185–189

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Sawada Y, Akiyama K, Sakata A, Kuwahara A, Otsuki H, Sakurai T, Saito K, Hirai MY (2009) Widely targeted metabolomics based on large-scale MS/MS data for elucidation metabolite accumulation patterns in plants. Plant Cell Physiol 50:37–47

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Shen W, Wei Y, Dauk M, Tan Y, Taylor DC, Selvarai G, Zou J (2006) Involvement of a glycerol-3-phosphate dehydrogenase in modulating the NADH/NAD+ ratio provides evidence of a mitochondrial glycerol-3-phosphate shuttle in Arabidopsis. Plant Cell 18:422–441

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Sulistyaningsih E, Tashiro Y, Shigyo M (1997) Morphological and cytological characteristics of haploid shallot. Bull Fac Agric Saga Univ 82:7–15

    Google Scholar 

  • Sulistyaningsih E, Aoyagi Y, Tashiro Y (2006) Flower bud culture of shallot (Allium cepa L. Aggregatum group) with cytogenetic analysis of resulting gynogenic plants and somaclones. Plant Cell Tissue Organ Cult 86:249–255

    Article  Google Scholar 

  • Taji T, Ohsumi C, Iuchi S, Seki M, Kasuga M, Kobayashi M, Yamaguchi-Shinozaki K, Shinozaki K (2002) Important roles of drought and cold inducible genes for galactinol synthase in stress tolerance in Arabidopsis thaliana. Plant J 29:417–426

    Article  CAS  PubMed  Google Scholar 

  • Takeda F, Matsuoka M (2008) Genetic approaches to crop improvement: responding to environmental and population changes. Nat Rev Genet 9:444–457

    Article  CAS  PubMed  Google Scholar 

  • Van de Poel B, Bulens I, Oppermann Y, Hertoq ML, Nicolai BM, Sauter M, Geeraerd AH (2013) S-adenosyl-l-methionine usage during climacteric ripping of tomato in relation to ethylene and polyamine biosynthesis and transmethylation capacity. Physiol Plant 148:176–188

    Article  PubMed  Google Scholar 

  • Williamson JD, Jennings DB, Guo WW, Pharr DM (2002) Sugar alcohols, salt stress and fungal resistance: polyols––multifunctional plant protection. J Am Soc Hort Sci 127:467–473

    CAS  Google Scholar 

  • Wood AJ (1999) Comparison of salt-induced osmotic adjustment and trigonelline accumulation in two soybean cultivars. Biol Plant 41:389–394

    Article  Google Scholar 

  • Wu ZJ, Irizarry RA, Gentleman R, Martinez-Murillo F, Spencer F (2004) A model-based background adjustment for oligonucleotide expression arrays. J Am Stat Assoc 99:909–917

    Article  Google Scholar 

  • Yaguchi S, McCallum J, Shaw M, Pither-Joyce M, Onodera S, Shiomi N, Yamauchi N, Shigyo M (2008) Biochemical and genetic analysis of carbohydrate accumulation in Allium cepa L. Plant Cell Physiol 49:730–739

    Article  CAS  PubMed  Google Scholar 

  • Zagorchev L, Seal CE, Kranner I, Odjakova M (2013) A central role for thiols in plant tolerance to abiotic stress. Int J Mol Sci 14:7405–7432

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Zeh M, Casazza AP, Kreft O, Roessner U, Bieberich K, Willmitzer L, Hoefgen R, Hesse H (2001) Antisense inhibition of threonine synthase leads to high methionine content in transgenic potato plants. Plant Physiol 127:792–802

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Zhao J, Wiiliams CC, Last RL (1998) Induction of Arabidopsis tryptophan pathway enzymes and camalexin by amino acid starvation, oxidative stress and an abiotic elicitor. Plant Cell 10:359–370

    PubMed Central  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This research was supported in part by Strategic Japan-New Zealand Cooperative Program on Functional Food (Developments of a Metabolic Atlas of Allium Vegetables to Enable Dissection of Functional Properties) from Japan Science and Technology Agency (JST).

Author information

Authors and Affiliations

  1. The United Graduate School of Agricultural Sciences, Tottori University, 4-101 Koyama-Minami, Tottori, 680-8553, Japan

    Mostafa Abdelrahman, Naoki Yamauchi & Masayoshi Shigyo

  2. RIKEN Center for Sustainable Resource Science, 1-7-22 Suehiro-cho, Tsurumi-ku, Yokohama, Kanagawa, 230-0045, Japan

    Yuji Sawada, Ryo Nakabayashi, Masami Yokota Hirai & Kazuki Saito

  3. Graduate School of Life Sciences, Tohoku University, 2-1-1 Katahira, Aoba-ku, Sendai, 980-8577, Japan

    Shusei Sato

  4. Kazusa DNA Research Institute, 2-6-7 Kazusa-Kamatari, Kisarazu, Chiba, 292-0818, Japan

    Shusei Sato & Hideki Hirakawa

  5. Botany Department, Faculty of Science, Aswan University, Aswan, 81528, Egypt

    Magdi El-Sayed

  6. Graduate School of Pharmaceutical Sciences, Chiba University, 1-8-1 Inohana, Chuo-ku, Chiba, 260-8675, Japan

    Kazuki Saito

  7. Department of Biological and Environmental Sciences, Faculty of Agriculture, Yamaguchi University, Yamaguchi, 753-8515, Japan

    Naoki Yamauchi & Masayoshi Shigyo

Authors
  1. Mostafa Abdelrahman
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yuji Sawada
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ryo Nakabayashi
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Shusei Sato
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Hideki Hirakawa
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Magdi El-Sayed
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Masami Yokota Hirai
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Kazuki Saito
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Naoki Yamauchi
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Masayoshi Shigyo
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Masayoshi Shigyo.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 16 kb)

Supplementary material 2 (DOCX 15 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Abdelrahman, M., Sawada, Y., Nakabayashi, R. et al. Integrating transcriptome and target metabolome variability in doubled haploids of Allium cepa for abiotic stress protection. Mol Breeding 35, 195 (2015). https://doi.org/10.1007/s11032-015-0378-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11032-015-0378-2

Keywords

Search

Navigation