Skip to main content
SpringerLink
Log in

Transcriptomic Profiling of Lathyrus sativus L. Metabolism of β-ODAP, a Neuroexcitatory Amino Acid Associated with Neurodegenerative Lower Limb Paralysis

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

Abstract

Grass pea (Lathyrus sativus L.) is a unique potential crop for marginal arid regions with untapped, exceptional biotic/abiotic stress tolerance, and high protein content seeds. High dietary intake of grass pea is associated with neurodegenerative lower limb paralysis, thought due to the compound β-N-oxalyl-L-α, β-diaminopropionic acid (β-ODAP). β-ODAP increases after seed germination and then decreases subsequently. To monitor changes in gene expression during seed germination, RNA sequencing was performed on seedlings at 2, 6, and 25 days after sowing. A total of 213,258 unigenes were detected, corresponding to 39,548 coding sequences. Extensive Gene Ontology and coexpression network analysis suggested that primary metabolism, particularly carbohydrates and sulfur, were correlated with β-ODAP content. Our results identified transcriptional profiles related to grass pea seedling development, and provide invaluable insight into mechanisms of β-ODAP accumulation and degradation. Defining the gene space is essential for intelligent genetic, biotechnological, and breeding efforts to reduce β-ODAP for human benefit.

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
Fig. 7
Fig. 8

Similar content being viewed by others

References

  • Akalu G, Tufvesson F, Jönsson C, Nai BM (1998) Physico-chemical characteristics and functional properties of starch and dietary fibre in grass pea seeds. Starch - Stärke 50:374–382

    Article  CAS  Google Scholar 

  • Almeida NF, Leitao ST, Krezdorn N, Rotter B, Winter P, Rubiales D, Vaz Patto MC (2014) Allelic diversity in the transcriptomes of contrasting rust-infected genotypes of Lathyrus sativus, a lasting resource for smart breeding. BMC Plant Biol 14:376

    Article  Google Scholar 

  • Almeida NF, Krezdorn N, Rotter B, Winter P, Rubiales D, Vaz Patto MC (2015) Lathyrus sativus transcriptome resistance response to Ascochyta lathyri investigated by deepSuperSAGE analysis. Front Plant Sci 6:178

    Article  Google Scholar 

  • Arslan M (2017) Diversity for vitamin and amino acid content in grass pea (Lathyrus sativus L.). Legume Research 40:803–810

    Google Scholar 

  • Audic S, Claverie JM (1997) The significance of digital gene expression profiles. Genome Res 7:986–995

    Article  CAS  Google Scholar 

  • Barkan A, Small I (2014) Pentatricopeptide repeat proteins in plants. Annu Rev Plant Biol 65:415–442

    Article  CAS  Google Scholar 

  • Crozet P et al (2014) Mechanisms of regulation of SNF1/AMPK/SnRK1 protein kinases. Front Plant Sci 5:190

    Article  Google Scholar 

  • Dixit GP, Parihar AK, Bohra A, Singh NP (2016) Achievements and prospects of grass pea (Lathyrus sativus L.) improvement for sustainable food production. The Crop Journal 4:407–416

    Article  Google Scholar 

  • Fuller T, Langfelder P, Presson A, Horvath S (2011) Review of weighted gene coexpression network analysis

  • Getahun H, Lambein F, Vanhoorne M, Van der Stuyft P (2003) Food-aid cereals to reduce neurolathyrism related to grass-pea preparations during famine. Lancet (London, England) 362:1808–1810

    Article  Google Scholar 

  • Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I, Adiconis X, Fan L, Raychowdhury R, Zeng Q, Chen Z, Mauceli E, Hacohen N, Gnirke A, Rhind N, di Palma F, Birren BW, Nusbaum C, Lindblad-Toh K, Friedman N, Regev A (2011) Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol 29:644–652

    Article  CAS  Google Scholar 

  • Hanbury C, White C, Mullan B, Siddique K (2000) A review of the potential of Lathyrus sativus L. and L. cicera L. grain for use as animal feed. Anim Feed Sci Technol 87:1–27

    Article  Google Scholar 

  • Hao X, Yang T, Liu R, Hu J, Yao Y, Burlyaeva M, Wang Y, Ren G, Zhang H, Wang D, Chang J, Zong X (2017) An RNA sequencing transcriptome analysis of grasspea (Lathyrus sativus L.) and development of SSR and KASP markers. Front Plant Sci 8:1873

    Article  Google Scholar 

  • Hu J, Chen G, Zhang H, Qian Q, Ding Y (2016) Comparative transcript profiling of alloplasmic male-sterile lines revealed altered gene expression related to pollen development in rice (Oryza sativa L.). BMC Plant Biol 16:175

    Article  Google Scholar 

  • Ikegami F, Itagaki S, Ishikawa T, Ongena G, Kuo YH, Lambein F, Murakoshi I (1991) Biosynthesis of beta-(isoxazolin-5-on-2-yl)alanine, the precursor of the neurotoxic amino acid beta-N-oxalyl-L-alpha,beta-diaminopropionic acid. Chemical and Pharmaceutical Bulletin (Tokyo) 39:3376–3377

    Article  CAS  Google Scholar 

  • Ikegami F, Horiuchi S, Kobori M, Morishige I, Murakoshi I (1992) Biosynthesis of neuroactive amino acids by cysteine synthases in Lathyrus latifolius. Phytochemistry 31:1991–1996

    Article  CAS  Google Scholar 

  • Ikegami F, Kamiya M, Kuo YH, Lambein F, Murakoshi I (1996) Enzymatic synthesis of two isoxazolylalanine isomers by cysteine synthases in Lathyrus species. Biol Pharm Bull 19:1214–1215

    Article  CAS  Google Scholar 

  • Jiao C-J, Xu Q-L, Wang C-Y, Li F-M, Li Z-X, Wang Y-F (2006) Accumulation pattern of toxin β-ODAP during lifespan and effect of nutrient elements on β-ODAP content in Lathyrus sativus seedlings. J Agric Sci 144:369–375

    Article  CAS  Google Scholar 

  • Jiao CJ, Jiang JL, Ke LM, Cheng W, Li FM, Li ZX, Wang CY (2011) Factors affecting beta-ODAP content in Lathyrus sativus and their possible physiological mechanisms. Food Chem Toxicol 49:543–549

    Article  CAS  Google Scholar 

  • Jiao CJ, Zhao FY, Xie SQ, Yuan JY, Yang LJ (2014) Assay for activities of cysteine synthase and β-cyanoalanine synthase. Amino Acid Biotic Resour 36:66–72

    CAS  Google Scholar 

  • Kohl M, Wiese S, Warscheid B (2011) Cytoscape: software for visualization and analysis of biological networks. In: Hamacher M, Eisenacher M, Stephan C (eds) Data mining in proteomics: from standards to applications. Humana Press, Totowa, pp 291–303

    Chapter  Google Scholar 

  • Krishnan HB (2005) Engineering soybean for enhanced sulfur amino acid content. Crop Sci 45:454–461

    Article  CAS  Google Scholar 

  • Kusama-Eguchi K, Yoshino N, Minoura A, Watanabe K, Kusama T, Lambein F, Ikegami F (2011) Sulfur amino acids deficiency caused by grass pea diet plays an important role in the toxicity of L-beta-ODAP by increasing the oxidative stress: studies on a motor neuron cell line. Food Chem Toxicol 49:636–643

    Article  CAS  Google Scholar 

  • Langfelder P, Horvath S (2008) WGCNA: an R package for weighted correlation network analysis. BMC Bioinformatics 9:559

    Article  Google Scholar 

  • Leustek T, Saito K (1999) Sulfate transport and assimilation in plants. Plant Physiol 120:637–644

    Article  CAS  Google Scholar 

  • Li A, Zhou M, Wei D, Chen H, You C, Lin J (2017) Transcriptome profiling reveals the negative regulation of multiple plant hormone signaling pathways elicited by overexpression of C-repeat binding factors. Front Plant Sci 8:1647

    Article  Google Scholar 

  • Liu F, Jiao C, Bi C, Xu Q, Chen P, Heuberger AL, Krishnan HB (2017) Metabolomics approach to understand mechanisms of β-N-oxalyl-l-α,β-diaminopropionic acid (β-ODAP) biosynthesis in grass pea (Lathyrus sativus L.). J Agric Food Chem 65:10206–10213

    Article  CAS  Google Scholar 

  • Main D et al. (2014) The cool season food legume database: an integrated resource for basic, translational and applied research. In: Proceedings of the international plant and animal genome conference. , San Diego, CA, USA

  • Manna S (2015) An overview of pentatricopeptide repeat proteins and their applications. Biochimie 113:93–99

    Article  CAS  Google Scholar 

  • Martinez-Barajas E, Delatte T, Schluepmann H, de Jong GJ, Somsen GW, Nunes C, Primavesi LF, Coello P, Mitchell RAC, Paul MJ (2011) Wheat grain development is characterized by remarkable trehalose 6-phosphate accumulation pregrain filling: tissue distribution and relationship to SNF1-related protein kinase1 activity. Plant Physiol 156:373–381

    Article  CAS  Google Scholar 

  • Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B (2008) Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Methods 5:621–628

    Article  CAS  Google Scholar 

  • Nunes C, Primavesi LF, Patel MK, Martinez-Barajas E, Powers SJ, Sagar R, Fevereiro PS, Davis BG, Paul MJ (2013) Inhibition of SnRK1 by metabolites: tissue-dependent effects and cooperative inhibition by glucose 1-phosphate in combination with trehalose 6-phosphate. Plant Physiol Biochem 63:89–98

    Article  CAS  Google Scholar 

  • Piattoni CV, Bustos DM, Guerrero SA, Iglesias AA (2011) Nonphosphorylating glyceraldehyde-3-phosphate dehydrogenase is phosphorylated in wheat endosperm at serine-404 by an SNF1-related protein kinase allosterically inhibited by ribose-5-phosphate. Plant Physiol 156:1337–1350

    Article  CAS  Google Scholar 

  • Rao SL, Adiga PR, Sarma PS (1964) The isolation and characterization of beta-n-oxalyl-l-alpha,beta-diaminopropionic acid: a neurotoxin from the seeds of Lathyrus sativus. Biochemistry 3:432–436

    Article  CAS  Google Scholar 

  • Spencer PS, Roy DN, Ludolph A, Hugon J, Dwivedi MP, Schaumburg HH (1986) Lathyrism: evidence for role of the neuroexcitatory aminoacid BOAA. Lancet (London, England) 2:1066–1067

    Article  CAS  Google Scholar 

  • Takahashi H, Saito K (1996) Subcellular localization of spinach cysteine synthase isoforms and regulation of their gene expression by nitrogen and sulfur. Plant Physiol 112:273–280

    Article  CAS  Google Scholar 

  • Tan R-Y et al (2017) Plant toxin β-ODAP activates integrin β1 and focal adhesion: a critical pathway to cause neurolathyrism. Sci Rep 7:40677

    Article  CAS  Google Scholar 

  • Trapnell C, Roberts A, Goff L, Pertea G, Kim D, Kelley DR, Pimentel H, Salzberg SL, Rinn JL, Pachter L (2012) Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat Protoc 7:562–578

    Article  CAS  Google Scholar 

  • Wan XL, Zhou Q, Wang YY, Wang WE, Bao MZ, Zhang JW (2015) Identification of heat-responsive genes in carnation (Dianthus caryophyllus L.) by RNA-seq. Front Plant Sci 6:519

    PubMed  PubMed Central  Google Scholar 

  • Xu Q, Liu F, Chen P, Jez JM, Krishnan HB (2017) β-N-oxalyl-l-α,β-diaminopropionic acid (β-ODAP) content in Lathyrus sativus: the integration of nitrogen and sulfur metabolism through β-cyanoalanine synthase. Int J Mol Sci 18:526

    Article  Google Scholar 

  • Yan ZY, Spencer PS, Li ZX, Liang YM, Wang YF, Wang CY, Li FM (2006) Lathyrus sativus (grass pea) and its neurotoxin ODAP. Phytochemistry 67:107–121

    Article  CAS  Google Scholar 

  • Yang T, Jiang J, Burlyaeva M, Hu J, Coyne CJ, Kumar S, Redden R, Sun X, Wang F, Chang J, Hao X, Guan J, Zong X (2014) Large-scale microsatellite development in grasspea (Lathyrus sativus L.), an orphan legume of the arid areas. BMC Plant Biol 14:65

    Article  Google Scholar 

  • Yang M, Zhu L, Li L, Li J, Xu L, Feng J, Liu Y (2017) Digital gene expression analysis provides insight into the transcript profile of the genes involved in aporphine alkaloid biosynthesis in lotus (Nelumbo nucifera). Front Plant Sci 8:80

    PubMed  PubMed Central  Google Scholar 

Download references

Funding

This study was supported by the National Natural Science Foundation (31401910), China Postdoctoral Science Foundation (2016M590975), Postdoctoral Science Foundation of Shaanxi province (2016BSHEDZZ119), and the Fundamental Research Funds for the Central Universities (2014YB040), P.R. China.

Author information

Authors and Affiliations

  1. College of Life Sciences, Northwest A&F University, Yangling, 712100, Shaanxi, China

    Quanle Xu, Fengjuan Liu, Ruihong Qu, Chunxiao Bi, Xin Hu & Peng Chen

  2. Plant Genetics Research Unit, USDA-Agricultural Research Service, University of Missouri, Columbia, MO, 65211, USA

    Jason D. Gillman & Hari B. Krishnan

Authors
  1. Quanle Xu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Fengjuan Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ruihong Qu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jason D. Gillman
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Chunxiao Bi
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Xin Hu
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Peng Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Hari B. Krishnan
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Quanle Xu, Peng Chen, and Hari Krishnan designed the study. Quanle Xu, Jason D. Gillman, Peng Chen, and Hari Krishnan wrote and edited the manuscript. Fengjuan Liu and Ruihong Qu performed qRT-PCR validation. Fengjuan Liu, Jason D. Gillman, Chunxiao Bi, and Xin Hu carried out bioinformatics analysis. All authors read and approved the final manuscript.

Corresponding authors

Correspondence to Peng Chen or Hari B. Krishnan.

Ethics declarations

Conflict of Interest

The authors declare that they have no conflict of interest.

Electronic supplementary material

Supplemental Table 1

(DOCX 15 kb)

Supplemental Figure 1

The quality of the transcriptome sequence assembly result and the size distribution. (PNG 286 kb)

High resolution image (TIF 531 kb)

Supplemental Figure 2

Top BLAST hit species distribution and summary of BLAST2GO annotation of coding sequences identified in Lathyrus sativus transcriptome. (PNG 271 kb)

High resolution image (TIF 438 kb)

Supplemental Figure 3

Weighted gene coexpression network analysis (WGCNA) of differentially expressed genes (DEGs). Cytoscape representation of coexpressed gene CS TR27757|c5_g1_i2 len = 1358. (PNG 1500 kb)

High resolution image (TIF 8865 kb)

Supplemental Figure 4

Weighted gene coexpression network analysis (WGCNA) of differentially expressed genes (DEGs). Cytoscape representation of coexpressed gene CS TR72159|c0_g1_i2 len = 1526. (PNG 170 kb)

High resolution image (TIF 4221 kb)

ESM 1

(XLSX 65328 kb)

ESM 2

(XLSX 45459 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Xu, Q., Liu, F., Qu, R. et al. Transcriptomic Profiling of Lathyrus sativus L. Metabolism of β-ODAP, a Neuroexcitatory Amino Acid Associated with Neurodegenerative Lower Limb Paralysis. Plant Mol Biol Rep 36, 832–843 (2018). https://doi.org/10.1007/s11105-018-1123-x

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11105-018-1123-x

Keywords

Search

Navigation