Abstract
Pyruvate decarboxylase (PDC) is the main enzyme in ethanol fermentation in plant low-oxygen response. Expression of the PDC gene can be induced by submergence, a low-oxygen state, which has been demonstrated in Arabidopsis, maize and rice among other plants. However, it is unknown whether the gene expression has similar pattern in the Fabaceae family under low-oxygen stress, and unavailability of PDC family member sequences in Fabaceae hindered these studies. We aimed to comprehensively identify PDC genes in adzuki bean, and characterize their phylogenetic relationships and expression profile with the emphasis of expression response to submergence. Based on genome sequences and identified conserved domains, HMMER was used to mine PDC genes in adzuki bean in addition to mung bean, both of which are Vigna species under the Fabaceae family. Sequences were aligned using MUSCLE and Phylogenetic topology was decided by using MrBayes. Tissue expression patterns were decided using publically available RNASeq data. Adzuki bean plants were treated with submergence stress, and expressions under treatments were measured using qRT-PCR. We identified the genes in PDC family in the genomes of adzuki bean and mung bean. The known PDC peptides contain three conserved domains with the same order. Based on the domain composition, we identified four PDC family genes in adzuki bean, and three in mung bean. Phylogenetic reconstruction resolved three major classes. Class I of the family was grouped with PDC gene in Arabidopsis, and thus likely encodes PDC; one gene is present in this class in adzuki bean, whose expression was high in roots and nodules compared to other tissues, and was significantly induced under submergence treatment, reaching highest at 12 h after waterlogging. No Class I gene was identified in mung bean, possibly result of assembly gaps or failure of gene model prediction of mung bean genome. Class II genes are clustered together with larger subunit of acetolactate synthase, which have two representatives in mung bean and adzuki bean, respectively. There is one copy of gene in Class III in the genome of the two Vigna species, respectively, which is grouped with an uncharacterized Arabidopsis gene. Interestingly, the adzuki bean gene in this class was significantly induced by waterlogging, whose expression reaching the highest earlier than the Class I gene, which indicates that both the Class I and Class III genes in the PDC family are involved in low-oxygen stress response in adzuki bean. Pyruvate decarboxylase family genes were mined in adzuki bean and mung bean, whose phylogeny was clarified into three independent classes. Expression of a putative PDC gene was significantly elevated by submergence stress in adzuki bean. The Class III gene in adzuki bean was significantly induced in expression by waterlogging, too, yet its expression reached highest earlier than putative PDC genes, suggesting involvement of the Class III genes in low-oxygen stress response.
Similar content being viewed by others
References
Arru L, Fornaciari S, Mancuso S (2014) New insights into the metabolic and molecular mechanism of plant response to anaerobiosis. Int Rev Cell Mol Biol 311:231–264. https://doi.org/10.1016/B978-0-12-800179-0.00005-2
Baier F, Copp JN, Tokuriki N (2016) Evolution of enzyme superfamilies: comprehensive exploration of sequence-function relationships. Biochemistry 55:6375–6388. https://doi.org/10.1021/acs.biochem.6b00723
Brown SD, Gerlt JA, Seffernick JL, Babbitt PC (2006) A gold standard set of mechanistically diverse enzyme superfamilies. Genome Biol 7:R8. https://doi.org/10.1186/gb-2006-7-1-r8
Camacho C, Coulouris G, Avagyan V, Ma N, Papadopoulos J, Bealer K, Madden TL (2009) BLAST+: architecture and applications. BMC Bioinformatics 10:421. https://doi.org/10.1186/1471-2105-10-421
Chang AK, Duggleby RG (1997) Expression, purification and characterization of Arabidopsis thaliana acetohydroxyacid synthase. Biochem J 327:161–169
Clifton BE, Kaczmarski JA, Carr PD, Gerth ML, Tokuriki N, Jackson CJ (2018) Evolution of cyclohexadienyl dehydratase from an ancestral solute-binding protein. Nat Chem Biol 14:542–547. https://doi.org/10.1038/s41589-018-0043-2
Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797. https://doi.org/10.1093/nar/gkh340
Finn RD, Coggill P, Eberhardt RY, Eddy SR, Mistry J, Mitchell AL, Potter SC, Punta M, Qureshi M, Sangrador-Vegas A, Salazar GA, Tate J, Bateman A (2016) The Pfam protein families database: towards a more sustainable future. Nucleic Acids Res 44:D279–D285. https://doi.org/10.1093/nar/gkv1344
Frohme M, Camargo AA, Czink C, Matsukuma AY, Simpson AJ, Hoheisel JD, Verjovski-Almeida S (2001) Directed gap closure in large-scale sequencing projects. Genome Res 11:901–903. https://doi.org/10.1101/gr.179401
Furnham N, Dawson NL, Rahman SA, Thornton JM, Orengo CA (2016) Large-scale analysis exploring evolution of catalytic machineries and mechanisms in enzyme superfamilies. J Mol Biol 428:253–267. https://doi.org/10.1016/j.jmb.2015.11.010
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(7):644–652. https://doi.org/10.1038/nbt.1883
Haas BJ, Delcher AL, Mount SM, Wortman JR, Smith RK Jr, Hannick LI, Maiti R, Ronning CM, Rusch DB, Town CD, Salzberg SL, White O (2003) Improving the Arabidopsis genome annotation using maximal transcript alignment assemblies. Nucleic Acids Res 31:5654–5666
Hartmann T (2007) From waste products to ecochemicals: fifty years research of plant secondary metabolism. Phytochemistry 68:2831–2846. https://doi.org/10.1016/j.phytochem.2007.09.017
Haughn GW, Somerville CR (1990) A mutation causing Imidazolinone resistance maps to the Csr1 locus of Arabidopsis thaliana. Plant Physiol 92:1081–1085
Huhta DW, Heckenthaler T, Alvarez FJ, Ermer J, Hubner G, Schellenberger A, Schowen RL (1992) The catalytic power of pyruvate decarboxylase. A stochastic model for the molecular evolution of enzymes. Acta Chem Scand 46:778–788
Ismond KP, Dolferus R, de Pauw M, Dennis ES, Good AG (2003) Enhanced low oxygen survival in Arabidopsis through increased metabolic flux in the fermentative pathway. Plant Physiol 132:1292–1302. https://doi.org/10.1104/pp.103.022244
Jander G, Joshi V (2009) Aspartate-derived amino acid biosynthesis in Arabidopsis thaliana. Arabidopsis Book 7:e0121. https://doi.org/10.1199/tab.0121
Kang YJ, Kim SK, Kim MY, Lestari P, Kim KH, Ha BK, Jun TH, Hwang WJ, Lee T, Lee J, Shim S, Yoon MY, Jang YE, Han KS, Taeprayoon P, Yoon N, Somta P, Tanya P, Kim KS, Gwag JG, Moon JK, Lee YH, Park BS, Bombarely A, Doyle JJ, Jackson SA, Schafleitner R, Srinives P, Varshney RK, Lee SH (2014) Genome sequence of mungbean and insights into evolution within Vigna species. Nat Commun 5:5443. https://doi.org/10.1038/ncomms6443
Kang YJ, Satyawan D, Shim S, Lee T, Lee J, Hwang WJ, Kim SK, Lestari P, Laosatit K, Kim KH, Ha TJ, Chitikineni A, Kim MY, Ko JM, Gwag JG, Moon JK, Lee YH, Park BS, Varshney RK, Lee SH (2015) Draft genome sequence of adzuki bean, Vigna angularis. Sci Rep 5:8069. https://doi.org/10.1038/srep08069
Kochevenko A, Araujo WL, Maloney GS, Tieman DM, Do PT, Taylor MG, Klee HJ, Fernie AR (2012) Catabolism of branched chain amino acids supports respiration but not volatile synthesis in tomato fruits. Mol Plant 5:366–375. https://doi.org/10.1093/mp/ssr108
Lonhienne T, Garcia MD, Pierens G, Mobli M, Nouwens A, Guddat LW (2018) Structural insights into the mechanism of inhibition of AHAS by herbicides. Proc Natl Acad Sci U S A 115:E1945–E1954. https://doi.org/10.1073/pnas.1714392115
Loreti E, Poggi A, Novi G, Alpi A, Perata P (2005) A genome-wide analysis of the effects of sucrose on gene expression in Arabidopsis seedlings under anoxia. Plant Physiol 137:1130–1138. https://doi.org/10.1104/pp.104.057299
Luo HT, Zhang JY, Wang G, Jia ZH, Huang SN, Wang T, Guo ZR (2017) Functional characterization of waterlogging and heat stresses tolerance gene pyruvate decarboxylase 2 from Actinidia deliciosa. Int J Mol Sci 18:2377. https://doi.org/10.3390/ijms18112377
Meng X, Ji Y (2013) Modern computational techniques for the HMMER sequence analysis. ISRN Bioinform 2013:252183. https://doi.org/10.1155/2013/252183
Mithran M, Paparelli E, Novi G, Perata P, Loreti E (2014) Analysis of the role of the pyruvate decarboxylase gene family in Arabidopsis thaliana under low-oxygen conditions. Plant Biol (Stuttg) 16:28–34. https://doi.org/10.1111/plb.12005
Ngaki MN, Louie GV, Philippe RN, Manning G, Pojer F, Bowman ME, Li L, Larsen E, Wurtele ES, Noel JP (2012) Evolution of the chalcone-isomerase fold from fatty-acid binding to stereospecific catalysis. Nature 485:530–533. https://doi.org/10.1038/nature11009
Peng C, Uygun S, Shiu SH, Last RL (2015) The impact of the branched-chain Ketoacid dehydrogenase complex on amino acid homeostasis in Arabidopsis. Plant Physiol 169:1807–1820. https://doi.org/10.1104/pp.15.00461
Poole RL (2007) The TAIR database. Methods Mol Biol 406:179–212
Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Hohna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61:539–542. https://doi.org/10.1093/sysbio/sys029
Sathasivan K, Haughn GW, Murai N (1990) Nucleotide sequence of a mutant acetolactate synthase gene from an imidazolinone-resistant Arabidopsis thaliana var. Columbia. Nucleic Acids Res 18:2188
Schmutz J, Cannon SB, Schlueter J, Ma J, Mitros T, Nelson W, Hyten DL, Song Q, Thelen JJ, Cheng J, Xu D, Hellsten U, May GD, Yu Y, Sakurai T, Umezawa T, Bhattacharyya MK, Sandhu D, Valliyodan B, Lindquist E, Peto M, Grant D, Shu S, Goodstein D, Barry K, Futrell-Griggs M, Abernathy B, Du J, Tian Z, Zhu L, Gill N, Joshi T, Libault M, Sethuraman A, Zhang XC, Shinozaki K, Nguyen HT, Wing RA, Cregan P, Specht J, Grimwood J, Rokhsar D, Stacey G, Shoemaker RC, Jackson SA (2010) Genome sequence of the palaeopolyploid soybean. Nature 463:178–183. https://doi.org/10.1038/nature08670
Stanke M, Steinkamp R, Waack S, Morgenstern B (2004) AUGUSTUS: a web server for gene finding in eukaryotes. Nucleic Acids Res 32:W309–W312. https://doi.org/10.1093/nar/gkh379
Valerio A, D'Antona G, Nisoli E (2011) Branched-chain amino acids, mitochondrial biogenesis, and healthspan: an evolutionary perspective. Aging (Albany NY) 3:464–478. https://doi.org/10.18632/aging.100322
Verhagen FH, Stigter ECA, Pras-Raves ML, Burgering BMT, Imhof SM, Radstake T, de Boer JH, Kuiper JJW (2018) Aqueous humor analysis identifies higher branched chain amino acid metabolism as a marker for HLA-B27 acute anterior uveitis and disease activity. Am J Ophthalmol 198:97–110. https://doi.org/10.1016/j.ajo.2018.10.004
Acknowledgments
The work is supported by Scientific Research and Service Platform Fund of Henan Province(2016151), the fund of scientific and technological innovation team of water ecological security for Water Source Region of Mid-line of South-to-North Diversion Project of Henan Province, and the National Natural Science Foundation of China (31671758).
Author information
Authors and Affiliations
Contributions
LY conceived and designed the study. JC, LM, PD, SY, HL and DC performed the experiments. JC, MZ, JY and LY analyzed the data. JC and LY wrote the paper. All authors read and approved the manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Chen, J., Ma, L., Duan, P. et al. Submergence response of pyruvate decarboxylase family genes in adzuki bean. Biologia 75, 1213–1220 (2020). https://doi.org/10.2478/s11756-020-00421-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.2478/s11756-020-00421-1