Genomics and biochemical analyses reveal a metabolon key to β-L-ODAP biosynthesis in Lathyrus sativus

. 2023 Feb 16 ; 14 (1) : 876. [epub] 20230216

Jazyk angličtina Země Anglie, Velká Británie Médium electronic

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid36797319

Grantová podpora
BBS/E/J/00000150 Biotechnology and Biological Sciences Research Council - United Kingdom
BBS/E/J/000PR9790 Biotechnology and Biological Sciences Research Council - United Kingdom

Odkazy

PubMed 36797319
PubMed Central PMC9935904
DOI 10.1038/s41467-023-36503-2
PII: 10.1038/s41467-023-36503-2
Knihovny.cz E-zdroje

Grass pea (Lathyrus sativus L.) is a rich source of protein cultivated as an insurance crop in Ethiopia, Eritrea, India, Bangladesh, and Nepal. Its resilience to both drought and flooding makes it a promising crop for ensuring food security in a changing climate. The lack of genetic resources and the crop's association with the disease neurolathyrism have limited the cultivation of grass pea. Here, we present an annotated, long read-based assembly of the 6.5 Gbp L. sativus genome. Using this genome sequence, we have elucidated the biosynthetic pathway leading to the formation of the neurotoxin, β-L-oxalyl-2,3-diaminopropionic acid (β-L-ODAP). The final reaction of the pathway depends on an interaction between L. sativus acyl-activating enzyme 3 (LsAAE3) and a BAHD-acyltransferase (LsBOS) that form a metabolon activated by CoA to produce β-L-ODAP. This provides valuable insight into the best approaches for developing varieties which produce substantially less toxin.

Erratum v

PubMed

Zobrazit více v PubMed

Gil, J. D. B., Cohn, A. S., Duncan, J., Newton, P. & Vermeulen, S. The resilience of integrated agricultural systems to climate change. WIREs Clim. Change8, e461 (2017).10.1002/wcc.461 DOI

Mustafa, M. A., Mayes, S. & Massawe, F. Crop Diversification Through a Wider Use of Underutilised Crops: A Strategy to Ensure Food and Nutrition Security in the Face of Climate Change. in Sustainable Solutions for Food Security: Combating Climate Change by Adaptation (eds. Sarkar, A., Sensarma, S. R. & vanLoon, G. W.) 125–149 (Springer International Publishing, 2019). 10.1007/978-3-319-77878-5_7.

Mabhaudhi, T. et al. Prospects of orphan crops in climate change. Planta250, 695–708 (2019). 10.1007/s00425-019-03129-y PubMed DOI PMC

Chivenge, P., Mabhaudhi, T., Modi, A. & Mafongoya, P. The Potential Role of Neglected and Underutilised Crop Species as Future Crops under Water Scarce Conditions in Sub-Saharan Africa. Int. J. Environ. Res. Public Health12, 5685 (2015). 10.3390/ijerph120605685 PubMed DOI PMC

Yadav, S. S., Bejiga, G., Brink, M. & Belay, G. Lathyrus sativus L. PROTA4U vol. 2017 http://www.prota4u.org/search.asp (2006).

Campbell, C. G. Grass pea: Lathyrus sativus L. Promoting the conservation and use of underutilized and neglected crops vol. 18 (International Plant Genetic Resources Institute, 1997).

Jiao, C.-J. J. et al. Factors affecting beta-ODAP content in Lathyrus sativus and their possible physiological mechanisms. Food Chem. Toxicol.49, 543–549 (2011). 10.1016/j.fct.2010.04.050 PubMed DOI

Drouin, P., Prëvost, D. & Antoun, H. Physiological adaptation to low temperatures of strains of Rhizobium leguminosarum bv. viciae associated with Lathyrus spp. FEMS Microbiol. Ecol.32, 111–120 (2000). PubMed

Girma, A., Tefera, B. & Dadi, L. Grass pea and neurolathyrism: farmers’ perception on its consumption and protective measure in North Shewa, Ethiopia. Food Chem. Toxicol.49, 668–672 (2011). 10.1016/j.fct.2010.08.040 PubMed DOI

Zhelyazkova, T., Pavlov, D., Delchev, G. & Stoyanova, A. Productivity and yield stability of six grain legumes in the moderate climatic conditions in Bulgaria. Scientific Papers. Ser. A. Agron.LIX, 478–487 (2016).

Silvestre, S., de Sousa Araújo, S., Vaz Patto, M. C. & Marques da Silva, J. Performance index: an expeditious tool to screen for improved drought resistance in the Lathyrus genus. J. Integr. plant Biol.56, 610–621 (2014). 10.1111/jipb.12186 PubMed DOI

Yang, H.-M. & Zhang, X.-Y. Considerations on the reintroduction of grass pea in China. Lathyrus lathyrism Newsl.4, 22–26 (2005).

Vaz Patto, M. C., Fernández‐Aparicio, M., Moral, A. & Rubiales, D. Characterization of resistance to powdery mildew (Erysiphe pisi) in a germplasm collection of Lathyrus sativus. Plant Breed.125, 308–310 (2006).10.1111/j.1439-0523.2006.01220.x DOI

Dufour, D. L. Assessing diet in populations at risk for konzo and neurolathyrism. Food Chem. Toxicol.49, 655–661 (2011). 10.1016/j.fct.2010.08.006 PubMed DOI

Kusama-Eguchi, K. et al. New insights into the mechanism of neurolathyrism: L-β-ODAP triggers [Ca2+]iaccumulation and cell death in primary motor neurons through transient receptor potential channels and metabotropic glutamate receptors. Food Chem. Toxicol.67, 113–122 (2014). 10.1016/j.fct.2014.02.021 PubMed DOI

Lambein, F., Travella, S., Kuo, Y.-H., Van Montagu, M. & Heijde, M. Grass pea (Lathyrus sativus L.): orphan crop, nutraceutical or just plain food? Planta10.1007/s00425-018-03084-0 (2019). PubMed

Kumar, S., Bejiga, G., Ahmed, S., Nakkoul, H. & Sarker, A. Genetic improvement of grass pea for low neurotoxin (β-ODAP) content. Food Chem. Toxicol.49, 589–600 (2011). 10.1016/j.fct.2010.06.051 PubMed DOI

Sawant, P. V., Jayade, V. S. & Patil, S. R. Line × tester analysis in Lathyrus. J. Food Legumes24, 41–45 (2011).

Chakrabarti, A., Santha, I. M. & Mehta, S. L. Molecular characterisation of low ODAP somaclones of Lathyrus sativus. J. Plant Biochem. Biotechnol.8, 25–29 (1999).10.1007/BF03263053 DOI

Santha, I. M. & Mehta, S. L. Development of low ODAP somaclones of Lathyrus sativus. Lathyrus lathyrism Newsletter2, 42 (2001).

Tsegaye, D., Tadesse, W. & Bayable, M. Performance of grass pea (Lathyrus sativus L.) somaclones at Adet, northwest Ethiopia. Lathyrus lathyrism Newsletter 4, 5–6 (2005).

Siddique, K. H. M., Hanbury, C. L. & Sarker, A. Registration of ‘Ceora’ Grass Pea Registration by CSSA. Crop Sci.46, 986 (2006).10.2135/cropsci2005.0131 DOI

Lambein, F., Khan, J. K., Kuo, Y. H., Campbell, C. G. & Briggs, C. J. Toxins in the seedlings of some varieties of grass pea (Lathyrus sativus). Nat. Toxins1, 246–249 (1993). 10.1002/nt.2620010408 PubMed DOI

Kuo, Y.-H. & Lambein, F. Biosynthesis of the neurotoxin β-N-oxalyl-α, β-diaminopropionic acid in callus tissue of Lathyrus sativus. Phytochemistry30, 3241–3244 (1991).10.1016/0031-9422(91)83184-M DOI

Ikegami, F., Yamamoto, A., Kuo, Y. H. & Lambein, F. Enzymatic formation of 2,3-diaminopropionic acid, the direct precursor of the neurotoxin beta-ODAP, in Lathyrus sativus. Biol. Pharm. Bull.22, 770–771 (1999). 10.1248/bpb.22.770 PubMed DOI

Ikegami, F. et al. Biosynthesis of β-(isoxazolin-5-on-2-yl)-l-alanine by cysteine synthase in Lathyrus sativus. Phytochemistry33, 93–98 (1993).10.1016/0031-9422(93)85402-D DOI

Malathi, K., Padmanab, G. & Sarma, P. S. Biosynthesis of beta-N-oxalyl-L-alpha,beta-diaminopropionic acid, Lathyrus sativus neurotoxin. Phytochemistry9, 1603–1609 (1970).10.1016/S0031-9422(00)85283-8 DOI

Doležel, J. et al. Plant Genome Size Estimation by Flow Cytometry: Inter-laboratory Comparison. Ann. Bot.82, 17–26 (1998).10.1093/oxfordjournals.aob.a010312 DOI

Ruan, J. & Li, H. Fast and accurate long-read assembly with wtdbg2. Nat. Methods17, 155–158 (2020). 10.1038/s41592-019-0669-3 PubMed DOI PMC

Li, H. Minimap2: pairwise alignment for nucleotide sequences. Bioinformatics34, 3094–3100 (2018). 10.1093/bioinformatics/bty191 PubMed DOI PMC

Li, H. Aligning sequence reads, clone sequences and assembly contigs with BWA-MEM. arXiv:1303.3997 [q-bio] (2013).

Edwards, Anne et al. Lathyrus sativus LS007 genome assembly and annotation Rbp1.0. https://zenodo.org/record/7390878 (2022).

Simão, F. A., Waterhouse, R. M., Ioannidis, P., Kriventseva, E. V. & Zdobnov, E. M. BUSCO: assessing genome assembly and annotation completeness with single-copy orthologs. Bioinformatics31, 3210–3212 (2015). 10.1093/bioinformatics/btv351 PubMed DOI

Laetsch, D. R. & Blaxter, M. L. BlobTools: Interrogation of genome assemblies. F1000 Res. 6, 1287 (2017).

Emmrich, P. M. F. Genetic improvement of grass pea (Lathyrus sativus) for low β-L-ODAP content. (University of East Anglia, 2017).

Emmrich, P. M. F. et al. Linking a rapid throughput plate-assay with high-sensitivity stable-isotope label LCMS quantification permits the identification and characterisation of low β-L-ODAP grass pea lines. BMC Plant Biol.19, 489 (2019). 10.1186/s12870-019-2091-5 PubMed DOI PMC

Lowe, T. M. & Eddy, S. R. tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res25, 955–964 (1997). 10.1093/nar/25.5.955 PubMed DOI PMC

Novák, P., Neumann, P. & Macas, J. Global analysis of repetitive DNA from unassembled sequence reads using RepeatExplorer2. Nat. Protoc.15, 3745–3776 (2020). 10.1038/s41596-020-0400-y PubMed DOI

Macas, J. et al. In Depth Characterization of Repetitive DNA in 23 Plant Genomes Reveals Sources of Genome Size Variation in the Legume Tribe Fabeae. PLoS ONE10, e0143424 (2015). 10.1371/journal.pone.0143424 PubMed DOI PMC

Vondrak, T. et al. Characterization of repeat arrays in ultra-long nanopore reads reveals frequent origin of satellite DNA from retrotransposon-derived tandem repeats. Plant J.101, 484–500 (2020). 10.1111/tpj.14546 PubMed DOI PMC

Song, Y. et al. β-Cyanoalanine Synthase Regulates the Accumulation of β-ODAP via Interaction with Serine Acetyltransferase in Lathyrus sativus. J. Agric. Food Chem.69, 1953–1962 (2021). 10.1021/acs.jafc.0c07542 PubMed DOI

Xu, Q., Liu, F., Chen, P., Jez, J. M. & Krishnan, H. B. 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 (2017). 10.3390/ijms18030526 PubMed DOI PMC

Chakraborty, S. et al. Tissue specific expression and in-silico characterization of a putative cysteine synthase gene from Lathyrus sativus L. Gene Expr. Patterns27, 128–134 (2018). 10.1016/j.gep.2017.12.001 PubMed DOI

Yan, Z. Y. et al. Lathyrus sativus (grass pea) and its neurotoxin ODAP. Phytochemistry67, 107–121 (2006). 10.1016/j.phytochem.2005.10.022 PubMed DOI

Kobylarz, M. J. et al. Synthesis of L-2,3-Diaminopropionic Acid, a Siderophore and Antibiotic Precursor. Chem. Biol.21, 379–388 (2014). 10.1016/j.chembiol.2013.12.011 PubMed DOI

Foster, J., Kim, H. U., Nakata, P. A. & Browse, J. A previously unknown oxalyl-CoA synthetase is important for oxalate catabolism in Arabidopsis. Plant Cell Online24, 1217–1229 (2012).10.1105/tpc.112.096032 PubMed DOI PMC

Foster, J., Luo, B. & Nakata, P. A. An oxalyl-CoA dependent pathway of oxalate catabolism plays a role in regulating calcium oxalate crystal accumulation and defending against oxalate-secreting phytopathogens in Medicago truncatula. Plos One11, e0149850 (2016). 10.1371/journal.pone.0149850 PubMed DOI PMC

Foster, J. & Nakata, P. A. An oxalyl-CoA synthetase is important for oxalate metabolism in Saccharomyces cerevisiae. FEBS Lett.588, 160–166 (2014). 10.1016/j.febslet.2013.11.026 PubMed DOI

Goldsmith, M. et al. The identification and characterization of an oxalyl-CoA synthetase from grass pea (Lathyrus sativus L.). RSC Chem. Biol.3, 320–333 (2022). 10.1039/D1CB00202C PubMed DOI PMC

Kushwah, N. S. et al. Identifcation and characterization of oxalyl-CoA synthetase gene(LsAAE3) in grasspea (Lathyrus sativus L.). J. Food Legumes35, 27–40 (2022).

Quayle, J. R. Chemical synthesis of oxalyl-coenzyme A and its enzymic reduction to glyxylate. Biochim Biophys. Acta57, 398–400 (1962). 10.1016/0006-3002(62)91142-3 PubMed DOI

Leitch, I. J., Johnston, E., Pellicer, J., Hidalgo, O. & Bennett M.D. Plant DNA C-values database, Release 7.1. https://data.kew.org/cvalues/ (2019).

Kreplak, J. et al. A reference genome for pea provides insight into legume genome evolution. Nat. Genet.51, 1411–1422 (2019). 10.1038/s41588-019-0480-1 PubMed DOI

Shafin, K. et al. Nanopore sequencing and the Shasta toolkit enable efficient de novo assembly of eleven human genomes. Nature Biotechnology 1–10 10.1038/s41587-020-0503-6 (2020). PubMed PMC

Kolmogorov, M., Yuan, J., Lin, Y. & Pevzner, P. A. Assembly of long, error-prone reads using repeat graphs. Nat. Biotechnol.37, 540–546 (2019). 10.1038/s41587-019-0072-8 PubMed DOI

Chen, Y. et al. Fast and accurate assembly of Nanopore reads via progressive error correction and adaptive read selection. bioRxiv 2020.02.01.930107 10.1101/2020.02.01.930107 (2020).

Bankevich, A. et al. SPAdes: A New Genome Assembly Algorithm and Its Applications to Single-Cell Sequencing. J. Comput Biol.19, 455–477 (2012). 10.1089/cmb.2012.0021 PubMed DOI PMC

Zimin, A, V. et al. The MaSuRCA genome assembler. Bioinformatics29, 2669–2677 (2013). 10.1093/bioinformatics/btt476 PubMed DOI PMC

Lavin, M., Herendeen, P. S. & Wojciechowski, M. F. Evolutionary Rates Analysis of Leguminosae Implicates a Rapid Diversification of Lineages during the Tertiary. Syst. Biol.54, 575–594 (2005). 10.1080/10635150590947131 PubMed DOI

Azani, N. et al. A new subfamily classification of the Leguminosae based on a taxonomically comprehensive phylogeny: The Legume Phylogeny Working Group (LPWG). TAXON66, 44–77 (2017).10.12705/661.3 DOI

Schaefer, H. et al. Systematics, biogeography, and character evolution of the legume tribe Fabeae with special focus on the middle-Atlantic island lineages. BMC Evolut. Biol.12, 250 (2012).10.1186/1471-2148-12-250 PubMed DOI PMC

Ghasem, K., Danesh-Gilevaei, M. & Aghaalikhani, M. Karyotypic and nuclear DNA variations in Lathyrus sativus (Fabaceae). Caryologia64, 42–54 (2011).10.1080/00087114.2011.10589763 DOI

Neumann, P., Požárková, D. & Macas, J. Highly abundant pea LTR retrotransposon Ogre is constitutively transcribed and partially spliced. Plant Mol. Biol.53, 399–410 (2003). 10.1023/B:PLAN.0000006945.77043.ce PubMed DOI

Neumann, P., Koblížková, A., Navrátilová, A. & Macas, J. Significant Expansion of Vicia pannonica Genome Size Mediated by Amplification of a Single Type of Giant Retroelement. Genetics173, 1047–1056 (2006). 10.1534/genetics.106.056259 PubMed DOI PMC

Macas, J. & Neumann, P. Ogre elements — A distinct group of plant Ty3/gypsy-like retrotransposons. Gene390, 108–116 (2007). 10.1016/j.gene.2006.08.007 PubMed DOI

Schenk, S. U. & Werner, D. β-(3-isoxazolin-5-on-2-yl)-alanine from Pisum: allelopathic properties and antimycotic bioassay. Phytochemistry30, 467–470 (1991).10.1016/0031-9422(91)83706-Q DOI

Rekhter, D. et al. Isochorismate-derived biosynthesis of the plant stress hormone salicylic acid. Science365, 498–502 (2019). 10.1126/science.aaw1720 PubMed DOI

Shockey, J. M., Fulda, M. S. & Browse, J. Arabidopsis Contains a Large Superfamily of Acyl-Activating Enzymes. Phylogenetic and Biochemical Analysis Reveals a New Class of Acyl-Coenzyme A Synthetases. Plant Physiol.132, 1065–1076 (2003). 10.1104/pp.103.020552 PubMed DOI PMC

Nobuta, K. et al. The GH3 acyl adenylase family member PBS3 regulates salicylic acid-dependent defense responses in Arabidopsis. Plant Physiol.144, 1144–1156 (2007). 10.1104/pp.107.097691 PubMed DOI PMC

Torrens-Spence, M. P. et al. PBS3 and EPS1 Complete Salicylic Acid Biosynthesis from Isochorismate in Arabidopsis. Mol. Plant12, 1577–1586 (2019). 10.1016/j.molp.2019.11.005 PubMed DOI

Goldsmith, M. et al. Identification and characterization of the key enzyme in the biosynthesis of the neurotoxin β-ODAP in grass pea. J. Biol. Chem. 101806 10.1016/j.jbc.2022.101806 (2022) . PubMed PMC

Christian, M. et al. Targeting DNA double-strand breaks with TAL effector nucleases. Genetics186, 757–761 (2010). 10.1534/genetics.110.120717 PubMed DOI PMC

Wang, H., La Russa, M. & Qi, L. S. CRISPR/Cas9 in Genome Editing and Beyond. Annu. Rev. Biochem.85, 227–264 (2016). 10.1146/annurev-biochem-060815-014607 PubMed DOI

Belhaj, K., Chaparro-Garcia, A., Kamoun, S. & Nekrasov, V. Plant genome editing made easy: targeted mutagenesis in model and crop plants using the CRISPR/Cas system. Plant Methods9, 39 (2013). 10.1186/1746-4811-9-39 PubMed DOI PMC

Henikoff, S., Till, B. J. & Comai, L. TILLING. Traditional mutagenesis meets functional genomics. Plant Physiol.135, 630–636 (2004). 10.1104/pp.104.041061 PubMed DOI PMC

Kumar, A. P. K. et al. TILLING by Sequencing (TbyS) for targeted genome mutagenesis in crops. Mol. Breed.37, 14 (2017).10.1007/s11032-017-0620-1 DOI

Campbell, C. G. & Briggs, C. J. Registration of low neurotoxin content Lathyrus germplasm LS 8246. Crop Sci.27, 821 (1987).10.2135/cropsci1987.0011183X002700040055x DOI

Zimmer, R. C. & Campbell, C. First report of Sclerotinia sclerotiorum on Lathyrus sativus. Can. Plant Dis. Surv.70, 17–18 (1990).

Hanbury, D. C., Siddique, K., Seymour, M., Jones, R. & MacLeod, B. Growing Ceora grass pea (Lathyrus sativus) in Western Australia. FarmNote58, (Government of Western Australia, 2005).

Dolezel, J., Greilhuber, J. & Suda, J. Estimation of nuclear DNA content in plants using flow cytometry. Nat. Protoc.2, 2233–2244 (2007). 10.1038/nprot.2007.310 PubMed DOI

Grabherr, M. G. et al. Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat. Biotechnol.29, 644–652 (2011). 10.1038/nbt.1883 PubMed DOI PMC

Li, B. & Dewey, C. N. RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinforma.12, 323 (2011).10.1186/1471-2105-12-323 PubMed DOI PMC

Durand, N. C. et al. Juicer Provides a One-Click System for Analyzing Loop-Resolution Hi-C Experiments. Cell Syst.3, 95–98 (2016). 10.1016/j.cels.2016.07.002 PubMed DOI PMC

Dudchenko, O. et al. De novo assembly of the Aedes aegypti genome using Hi-C yields chromosome-length scaffolds. Science356, 92–95 (2017). 10.1126/science.aal3327 PubMed DOI PMC

Durand, N. C. et al. Juicebox Provides a Visualization System for Hi-C Contact Maps with Unlimited Zoom. Cell Syst.3, 99–101 (2016). 10.1016/j.cels.2015.07.012 PubMed DOI PMC

Venturini, L., Kaithakottil, G. & Swarbreck, D. Extended methods for the annotation of Triticum aestivum CS42. Earlham Institute, Norwich, UK (2016).

Danecek, P. et al. Twelve years of SAMtools and BCFtools. Gigascience10, giab008 (2021). 10.1093/gigascience/giab008 PubMed DOI PMC

Camacho, C. et al. BLAST+: architecture and applications. BMC Bioinforma.10, 421 (2009).10.1186/1471-2105-10-421 PubMed DOI PMC

Jones, P. et al. InterProScan 5: genome-scale protein function classification. Bioinformatics30, 1236–1240 (2014). 10.1093/bioinformatics/btu031 PubMed DOI PMC

Edgar, R. C. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res32, 1792–1797 (2004). 10.1093/nar/gkh340 PubMed DOI PMC

Waterhouse, A. M., Procter, J. B., Martin, D. M. A., Clamp, M. & Barton, G. J. Jalview Version 2–a multiple sequence alignment editor and analysis workbench. Bioinformatics25, 1189–1191 (2009). 10.1093/bioinformatics/btp033 PubMed DOI PMC

Stamatakis, A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics30, 1312–1313 (2014). 10.1093/bioinformatics/btu033 PubMed DOI PMC

Neumann, P., Novák, P., Hoštáková, N. & Macas, J. Systematic survey of plant LTR-retrotransposons elucidates phylogenetic relationships of their polyprotein domains and provides a reference for element classification. Mob. DNA10, 1 (2019). 10.1186/s13100-018-0144-1 PubMed DOI PMC

Kapust, R. B., Tözsér, J., Copeland, T. D. & Waugh, D. S. The P1′ specificity of tobacco etch virus protease. Biochemical Biophysical Res. Commun.294, 949–955 (2002).10.1016/S0006-291X(02)00574-0 PubMed DOI

Challis, R. rjchallis/assembly-stats. (2020).

Nejnovějších 20 citací...

Zobrazit více v
Medvik | PubMed

A chromosome-scale reference genome of grasspea (Lathyrus sativus)

. 2024 Sep 27 ; 11 (1) : 1035. [epub] 20240927

Najít záznam

Citační ukazatele

Nahrávání dat ...

    Možnosti archivace