Abstract
Key message
The study shows the biochemical and enzymatic divergence between the two aldehyde-alcohol dehydrogenases of the alga Polytomella sp., shedding light on novel aspects of the enzyme evolution amid unicellular eukaryotes.
Abstract
Aldehyde-alcohol dehydrogenases (ADHEs) are large metalloenzymes that typically perform the two-step reduction of acetyl-CoA into ethanol. These enzymes consist of an N-terminal acetylating aldehyde dehydrogenase domain (ALDH) and a C-terminal alcohol dehydrogenase (ADH) domain. ADHEs are present in various bacterial phyla as well as in some unicellular eukaryotes. Here we focus on ADHEs in microalgae, a diverse and polyphyletic group of plastid-bearing unicellular eukaryotes. Genome survey shows the uneven distribution of the ADHE gene among free-living algae, and the presence of two distinct genes in various species. We show that the non-photosynthetic Chlorophyte alga Polytomella sp. SAG 198.80 harbors two genes for ADHE-like enzymes with divergent C-terminal ADH domains. Immunoblots indicate that both ADHEs accumulate in Polytomella cells growing aerobically on acetate or ethanol. ADHE1 of ~ 105-kDa is found in particulate fractions, whereas ADHE2 of ~ 95-kDa is mostly soluble. The study of the recombinant enzymes revealed that ADHE1 has both the ALDH and ADH activities, while ADHE2 has only the ALDH activity. Phylogeny shows that the divergence occurred close to the root of the Polytomella genus within a clade formed by the majority of the Chlorophyte ADHE sequences, next to the cyanobacterial clade. The potential diversification of function in Polytomella spp. unveiled here likely took place after the loss of photosynthesis. Overall, our study provides a glimpse at the complex evolutionary history of the ADHE in microalgae which includes (i) acquisition via different gene donors, (ii) gene duplication and (iii) independent evolution of one of the two enzymatic domains.
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Data availability
The ADHE1 cDNA sequence can be found in the DDBJ/EMBL/GenBank databases under the accession number ERP116271.
References
Armbrust EV, Berges JA, Bowler C, Green BR, Martinez D, Putnam NH, Zhou S, Allen AE, Apt KE, Bechner M, Brzezinski MA, Chaal BK, Chiovitti A, Davis AK, Demarest MS, Detter JC, Glavina T, Goodstein D, Hadi MZ, Hellsten U, Hildebrand M, Jenkins BD, Jurka J, Kapitonov VV, Kröger N, Lau WWY, Lane TW, Larimer FW, Lippmeier JC, Lucas S, Medina M, Montsant A, Obornik M, Parker MS, Palenik B, Pazour GJ, Richardson PM, Rynearson TA, Saito MA, Schwartz DC, Thamatrakoln K, Valentin K, Vardi A, Wilkerson FP, Rokhsar DS (2004) The genome of the diatom Thalassiosira pseudonana: ecology, evolution, and metabolism. Science 306:79–86. https://doi.org/10.1126/science.1101156
Atteia A, Dreyfus G, González-Halphen D (1997) Characterization of the alpha and beta-subunits of the F0F1-ATPase from the alga Polytomella spp., a colorless relative of Chlamydomonas reinhardtii. Biochim Biophys Acta 1320:275–284. https://doi.org/10.1016/s0005-2728(97)00031-5
Atteia A, van Lis R, Ramírez J, González-Halphen D (2000) Polytomella spp. growth on ethanol. Extracellular pH affects the accumulation of mitochondrial cytochrome c550. Eur J Biochem 267:2850–2858. https://doi.org/10.1046/j.1432-1327.2000.01288.x
Atteia A, van Lis R, Mendoza-Hernández G, Henze K, Martin W, Riveros-Rosas H, González-Halphen D (2003) Bifunctional aldehyde/alcohol dehydrogenase (ADHE) in chlorophyte algal mitochondria. Plant Mol Biol 53:175–188. https://doi.org/10.1023/B:PLAN.0000009274.19340.36
Atteia A, van Lis R, Gelius-Dietrich G, Adrait A, Garin J, Joyard J, Rolland N, Martin W (2006) Pyruvate formate-lyase and a novel route of eukaryotic ATP synthesis in Chlamydomonas mitochondria. J Biol Chem 281:9909–9918. https://doi.org/10.1074/jbc.M507862200
Atteia A, van Lis R, Tielens AGM, Martin WF (2013) Anaerobic energy metabolism in unicellular photosynthetic eukaryotes. Biochim Biophys Acta Bioenerg 1827:210–223. https://doi.org/10.1016/j.bbabio.2012.08.002
Bairoch A (1992) Prosite: a dictionary of sites and patterns in proteins. Nucleic Acids Res 20:2013–2018. https://doi.org/10.1093/nar/20.suppl.2013
Blaby-Haas CE, Merchant SS (2019) Comparative and functional algal genomics. Annu Rev Plant Biol 70:605–638. https://doi.org/10.1146/annurev-arplant-050718-095841
Bouyssié D, Hesse A-M, Mouton-Barbosa E, Rompais M, Macron C, Carapito C, Gonzalez de Peredo A, Couté Y, Dupierris V, Burel A, Menetrey J-P, Kalaitzakis A, Poisat J, Romdhani A, Burlet-Schiltz O, Cianférani S, Garin J, Bruley C (2020) Proline: an efficient and user-friendly software suite for large-scale proteomics. Bioinformatics 36(10):3148–3155. https://doi.org/10.1093/bioinformatics/btaa118
Boxma B, Voncken F, Jannink S, van Alen T, Akhmanova A, van Weelden SWH, van Hellemond JJ, Ricard G, Huynen M, Tielens AGM, Hackstein JHP (2004) The anaerobic chytridiomycete fungus Piromyces sp. E2 produces ethanol via pyruvate:formate lyase and an alcohol dehydrogenase E. Mol Microbiol 51:1389–1399. https://doi.org/10.1046/j.1365-2958.2003.03912.x
Bruchhaus I, Tannich E (1994) Purification and molecular characterization of the NAD(+)-dependent acetaldehyde/alcohol dehydrogenase from Entamoeba histolytica. Biochem J 303(Pt 3):743–748. https://doi.org/10.1042/bj3030743
Burton RM, Stadtman ER (1953) The oxidation of acetaldehyde to acetyl coenzyme A. J Biol Chem 202:873–890
Catalanotti C, Dubini A, Subramanian V, Yang W, Magneschi L, Mus F, Seibert M, Posewitz MC, Grossman AR (2012) Altered fermentative metabolism in Chlamydomonas reinhardtii mutants lacking pyruvate formate lyase and both pyruvate formate lyase and alcohol dehydrogenase. Plant Cell 24:692–707. https://doi.org/10.1105/tpc.111.093146
Cederbaum AI, Lieber CS, Rubin E (1973) Effect of acetaldehyde on activity of shuttles for the transport of reducing equivalents into the mitochondria. FEBS Lett 37:89–92. https://doi.org/10.1016/0014-5793(73)80432-6
Cederbaum AI, Lieber CS, Rubin E (1974) The effect of acetaldehyde on mitochondrial function. Arch Biochem Biophys 161:26–39. https://doi.org/10.1016/0003-9861(74)90231-8
Copley SD (2020) Evolution of new enzymes by gene duplication and divergence. FEBS J 287:1262–1283. https://doi.org/10.1111/febs.15299
Emanuelsson O, Nielsen H, Brunak S, von Heijne G (2000) Predicting subcellular localization of proteins based on their N-terminal amino acid sequence. J Mol Biol 300:1005–1016. https://doi.org/10.1006/jmbi.2000.3903
Fukasawa Y, Tsuji J, Fu S-C, Tomii K, Horton P, Imai K (2015) MitoFates: improved prediction of mitochondrial targeting sequences and their cleavage sites. Mol Cell Proteomics 14:1113–1126. https://doi.org/10.1074/mcp.M114.043083
Funes S, Davidson E, Gonzalo Claros M, van Lis R, Pérez-Martínez X, Vázquez-Acevedo M, King MP, González-Halphen D (2002) The typically mitochondrial DNA-encoded ATP6 subunit of the F 1 F 0 -ATPase is encoded by a nuclear gene in Chlamydomonas reinhardtii. J Biol Chem 277:6051–6058. https://doi.org/10.1074/jbc.M109993200
Gould SB, Garg SG, Handrich M, Nelson-Sathi S, Gruenheit N, Tielens AGM, Martin WF (2019) Adaptation to life on land at high O(2) via transition from ferredoxin-to NADH-dependent redox balance. Proc Biol Sci 286:20191491. https://doi.org/10.1098/rspb.2019.1491
Guarnieri MT, Levering J, Henard CA, Boore JL, Betenbaugh MJ, Zengler K, Knoshaug EP (2018) Genome sequence of the oleaginous green alga, Chlorella vulgaris UTEX 395. Front Bioeng Biotechnol 6:37. https://doi.org/10.3389/fbioe.2018.00037
Hemschemeier A, Jacobs J, Happe T (2008) Biochemical and physiological characterization of the pyruvate formate-lyase Pfl1 of Chlamydomonas reinhardtii a typically bacterial enzyme in a eukaryotic alga. Eukaryot Cell 7:518–526. https://doi.org/10.1128/EC.00368-07
Jones DT, Taylor WR, Thornton JM (1992) The rapid generation of mutation data matrices from protein sequences. Bioinformatics 8:275–282. https://doi.org/10.1093/bioinformatics/8.3.275
Kawata T, Masuda K, Yoshino K (1975) Presence of fine spirals (spirosomes) in Lactobacillus fermenti and Lactobacillus casei. Jpn J Microbiol 19:225–227. https://doi.org/10.1111/j.1348-0421.1975.tb00872.x
Kessler D, Leibrecht I, Knappe J (1991) Pyruvate-formate-lyase-deactivase and acetyl-CoA reductase activities of Escherichia coli reside on a polymeric protein particle encoded by adhE. FEBS Lett 281:59–63. https://doi.org/10.1016/0014-5793(91)80358-a
Kessler D, Herth W, Knappe J (1992) Ultrastructure and pyruvate formate-lyase radical quenching property of the multienzymic AdhE protein of Escherichia coli. J Biol Chem 267:18073–18079
Kim KM, Park J-H, Bhattacharya D, Yoon HS (2014) Applications of next-generation sequencing to unravelling the evolutionary history of algae. Int J Syst Evol Microbiol 64:333–345. https://doi.org/10.1099/ijs.0.054221-0
Kim G, Azmi L, Jang S, Jung T, Hebert H, Roe AJ, Byron O, Song J-J (2019) Aldehyde-alcohol dehydrogenase forms a high-order spirosome architecture critical for its activity. Nat Commun 10:4527. https://doi.org/10.1038/s41467-019-12427-8
Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33(7):1870–1874. https://doi.org/10.1093/molbev/msw054
Kurylo CM, Parks MM, Juette MF, Zinshteyn B, Altman RB, Thibado JK, Vincent CT, Blanchard SC (2018) Endogenous rRNA sequence variation can regulate stress response gene expression and phenotype. Cell Rep 25:236-248.e6. https://doi.org/10.1016/j.celrep.2018.08.093
Lees GJ, Jago GR (1978) Role of acetaldehyde in metabolism: a review 1. Enzymes catalyzing reactions involving acetaldehyde. J Dairy Sci 61:1205–1215. https://doi.org/10.3168/jds.S0022-0302(78)83708-4
Magneschi L, Catalanotti C, Subramanian V, Dubini A, Yang W, Mus F, Posewitz MC, Seibert M, Perata P, Grossman AR (2012) A mutant in the ADH1 gene of Chlamydomonas reinhardtii elicits metabolic restructuring during anaerobiosis. Plant Physiol 158:1293–1305. https://doi.org/10.1104/pp.111.191569
Merchant SS, Prochnik SE, Vallon O, Harris EH, Karpowicz SJ, Witman GB, Terry A, Salamov A, Fritz-Laylin LK, Maréchal-Drouard L, Marshall WF, Qu LH, Nelson DR, Sanderfoot AA, Spalding MH, Kapitonov VV, Ren Q, Ferris P, Lindquist E, Shapiro H, Lucas SM, Grimwood J, Schmutz J, Grigoriev IV, Rokhsar DS, Grossman AR, Cardol P, Cerutti H, Chanfreau G, Chen CL, Cognat V, Croft MT, Dent R, Dutcher S, Fernández E, Fukuzawa H, González-Ballester D, González-Halphen D, Hallmann A, Hanikenne M, Hippler M, Inwood W, Jabbari K, Kalanon M, Kuras R, Lefebvre PA, Lemaire SD, Lobanov AV, Lohr M, Manuell A, Meier I, Mets L, Mittag M, Mittelmeier T, Moroney JV, Moseley J, Napoli C, Nedelcu AM, Niyogi K, Novoselov SV, Paulsen IT, Pazour G, Purton S, Ral JP, Riaño-Pachón DM, Riekhof W, Rymarquis L, Schroda M, Stern D, Umen J, Willows R, Wilson N, Zimmer SL, Allmer J, Balk J, Bisova K, Chen CJ, Elias M, Gendler K, Hauser C, Lamb MR, Ledford H, Long JC, Minagawa J, Page MD, Pan J, Pootakham W, Roje S, Rose A, Stahlberg E, Terauchi AM, Yang P, Ball S, Bowler C, Dieckmann CL, Gladyshev VN, Green P, Jorgensen R, Mayfield S, Mueller-Roeber B, Rajamani S, Sayre RT, Brokstein P, Dubchak I, Goodstein D, Hornick L, Huang YW, Jhaveri J, Luo Y, Martínez D, Ngau WCA, Otillar B, Poliakov A, Porter A, Szajkowski L, Werner G, Zhou K (2007) The Chlamydomonas genome reveals the evolution of key animal and plant functions. Science 318:245–251. https://doi.org/10.1126/science.1143609
Montella C, Bellsolell L, Pérez-Luque R, Badía J, Baldoma L, Coll M, Aguilar J (2005) Crystal structure of an iron-dependent group III dehydrogenase that interconverts L-lactaldehyde and L-1,2-propanediol in Escherichia coli. J Bacteriol 187:4957–4966. https://doi.org/10.1128/JB.187.14.4957-4966.2005
Müller M, Mentel M, van Hellemond JJ, Henze K, Woehle C, Gould SB, Yu R-Y, van der Giezen M, Tielens AGM, Martin WF (2012) Biochemistry and evolution of anaerobic energy metabolism in eukaryotes. Microbiol Mol Biol Rev 76:444–495. https://doi.org/10.1128/MMBR.05024-11
Mus F, Dubini A, Seibert M, Posewitz MC, Grossman AR (2007) Anaerobic acclimation in Chlamydomonas reinhardtii: anoxic gene expression, hydrogenase induction, and metabolic pathways. J Biol Chem 282:25475–25486. https://doi.org/10.1074/jbc.M701415200
Nelson DR, Chaiboonchoe A, Fu W, Hazzouri KM, Huang Z, Jaiswal A, Daakour S, Mystikou A, Arnoux M, Sultana M, Salehi-Ashtiani K (2019) Potential for heightened sulfur-metabolic capacity in coastal subtropical microalgae. Science 11:450–465. https://doi.org/10.1016/j.isci.2018.12.035
Pietrocola F, Galluzzi L, Bravo-San Pedro JM, Madeo F, Kroemer G (2015) Acetyl coenzyme A: a central metabolite and second messenger. Cell Metab 21:805–821. https://doi.org/10.1016/j.cmet.2015.05.014
Piganeau G, Grimsley N, Moreau H (2011) Genome diversity in the smallest marine photosynthetic eukaryotes. Res Microbiol 162:570–577. https://doi.org/10.1016/j.resmic.2011.04.005
Pony P, Rapisarda C, Terradot L, Marza E, Fronzes R (2020) Filamentation of the bacterial bi-functional alcohol/aldehyde dehydrogenase AdhE is essential for substrate channeling and enzymatic regulation. Nat Commun 11:1426. https://doi.org/10.1038/s41467-020-15214-y
Pringsheim EG (1955) The Genus Polytomella*. J Protozool 2:137–145. https://doi.org/10.1111/j.1550-7408.1955.tb02413.x
Radakovits R, Jinkerson RE, Fuerstenberg SI, Tae H, Settlage RE, Boore JL, Posewitz MC (2012) Draft genome sequence and genetic transformation of the oleaginous alga Nannochloropis gaditana. Nat Commun 3:686. https://doi.org/10.1038/ncomms1688
Roof DM, Roth JR (1992) Autogenous regulation of ethanolamine utilization by a transcriptional activator of the eut operon in Salmonella typhimurium. J Bacteriol 174:6634–6643. https://doi.org/10.1128/jb.174.20.6634-6643.1992
Rosenthal B, Mai Z, Caplivski D, Ghosh S, de la Vega H, Graf T, Samuelson J (1997) Evidence for the bacterial origin of genes encoding fermentation enzymes of the amitochondriate protozoan parasite Entamoeba histolytica. J Bacteriol 179:3736–3745. https://doi.org/10.1128/jb.179.11.3736-3745.1997
Salvetti A, Couté Y, Epstein A, Arata L, Kraut A, Navratil V, Bouvet P, Greco A (2016) Nuclear functions of nucleolin through global proteomics and interactomic approaches. J Proteome Res 15:1659–1669. https://doi.org/10.1021/acs.jproteome.6b00126
Sánchez LB (1998) Aldehyde dehydrogenase (CoA-acetylating) and the mechanism of ethanol formation in the amitochondriate protist, Giardia lamblia. Arch Biochem Biophys 354:57–64. https://doi.org/10.1006/abbi.1998.0664
Schägger H, von Jagow G (1991) Blue native electrophoresis for isolation of membrane protein complexes in enzymatically active form. Anal Biochem 199:223–231. https://doi.org/10.1016/0003-2697(91)90094-a
Schägger H, Cramer WA, von Jagow G (1994) Analysis of molecular masses and oligomeric states of protein complexes by blue native electrophoresis and isolation of membrane protein complexes by two-dimensional native electrophoresis. Anal Biochem 217:220–230. https://doi.org/10.1006/abio.1994.1112
Schwanhäusser B, Busse D, Li N, Dittmar G, Schuchhardt J, Wolf J, Chen W, Selbach M (2011) Global quantification of mammalian gene expression control. Nature 473:337–342. https://doi.org/10.1038/nature10098
Shasmal M, Dey S, Shaikh TR, Bhakta S, Sengupta J (2016) E. coli metabolic protein aldehyde-alcohol dehydrogenase-E binds to the ribosome: a unique moonlighting action revealed. Sci Rep 6:19936. https://doi.org/10.1038/srep19936
Small I, Peeters N, Legeai F, Lurin C (2004) Predotar: A tool for rapidly screening proteomes for N-terminal targeting sequences. Proteomics 4:1581–1590. https://doi.org/10.1002/pmic.200300776
Smith DR, Lee RW (2014) A plastid without a genome: evidence from the nonphotosynthetic green algal genus Polytomella. Plant Physiol 164:1812–1819. https://doi.org/10.1104/pp.113.233718
Smith DR, Hua J, Archibald JM, Lee RW (2013) Palindromic genes in the linear mitochondrial genome of the nonphotosynthetic green alga Polytomella magna. Genome Biol Evol 5:1661–1667. https://doi.org/10.1093/gbe/evt122
Studier FW (2005) Protein production by auto-induction in high density shaking cultures. Protein Expr Purif 41:207–234. https://doi.org/10.1016/j.pep.2005.01.016
Tardif M, Atteia A, Specht M, Cogne G, Rolland N, Brugière S, Hippler M, Ferro M, Bruley C, Peltier G, Vallon O, Cournac L (2012) PredAlgo: a new subcellular localization prediction tool dedicated to green algae. Mol Biol Evol 29:3625–3639. https://doi.org/10.1093/molbev/mss178
Toth J, Ismaiel AA, Chen JS (1999) The ald gene, encoding a coenzyme A-acylating aldehyde dehydrogenase, distinguishes Clostridium beijerinckii and two other solvent-producing clostridia from Clostridium acetobutylicum. Appl Environ Microbiol 65:4973–4980
van Lis R, González-Halphen D, Atteia A (2005) Divergence of the mitochondrial electron transport chains from the green alga Chlamydomonas reinhardtii and its colorless close relative Polytomella sp. Biochim Biophys Acta 1708:23–34. https://doi.org/10.1016/j.bbabio.2004.12.010
van Lis R, Mendoza-Hernández G, Groth G, Atteia A (2007) New insights into the unique structure of the F0F 1-ATP synthase from the chlamydomonad algae Polytomella sp. and Chlamydomonas reinhardtii. Plant Physiol 144:1190–1199. https://doi.org/10.1104/pp.106.094060
van Lis R, Baffert C, Couté Y, Nitschke W, Atteia A (2013) Chlamydomonas reinhardtii chloroplasts contain a homodimeric pyruvate: ferredoxin oxidoreductase that functions with FDX1. Plant Physiol 161:57–71. https://doi.org/10.1104/pp.112.208181
van Lis R, Popek M, Couté Y, Kosta A, Drapier D, Nitschke W, Atteia A (2017) Concerted up-regulation of aldehyde/alcohol dehydrogenase (ADHE) and starch in Chlamydomonas reinhardtii increases survival under dark anoxia. J Biol Chem 292:2395–2410. https://doi.org/10.1074/jbc.M116.766048
van Lis R, Brugière S, Baffert C, Couté Y, Nitschke W, Atteia A (2020) Hybrid cluster proteins in a photosynthetic microalga. FEBS J 287:721–735. https://doi.org/10.1111/febs.15025
Wang D, Ning K, Li J, Hu J, Han D, Wang H, Zeng X, Jing X, Zhou Q, Su X, Chang X, Wang A, Wang W, Jia J, Wei L, Xin Y, Qiao Y, Huang R, Chen J, Han B, Yoon K, Hill RT, Zohar Y, Chen F, Hu Q, Xu J (2014) Nannochloropsis genomes reveal evolution of microalgal oleaginous traits. PLoS Genet 10:e1004094. https://doi.org/10.1371/journal.pgen.1004094
Wessel D, Flügge UI (1984) A method for the quantitative recovery of protein in dilute solution in the presence of detergents and lipids. Anal Biochem 138:141–143. https://doi.org/10.1016/0003-2697(84)90782-6
Wise DL (1955) Carbon sources for Polytomella caeca. J Protozool 2:156–158. https://doi.org/10.1111/j.1550-7408.1955.tb02416.x
Wise DL (1959) Carbon nutrition and metabolism of Polytomella caeca. J Protozool 6:19–23. https://doi.org/10.1111/j.1550-7408.1959.tb03921.x
Wise DL (1968) Effects of acetaldehyde on growth and biosynthesis in an algal flagellate Polytomella caeca. J Protozool 15:528–531. https://doi.org/10.1111/j.1550-7408.1968.tb02169.x
Wise DL (1970) Effect of acetaldehyde on growth in succinate media and labeling RNA with 14C succinate in Polytomella caeca. J Protozool 17:1970
Wu T, Li L, Jiang X, Yang Y, Song Y, Chen L, Xu X, Shen Y, Gu Y (2019) Sequencing and comparative analysis of three Chlorella genomes provide insights into strain-specific adaptation to wastewater. Sci Rep 9:9514. https://doi.org/10.1038/s41598-019-45511-6
Zimorski V, Martin WF (2014) Subcellular targeting of proteins and pathways during evolution. New Phytol 201:1–2. https://doi.org/10.1111/nph.12566
Acknowledgements
We thank Dr. David R. Smith (Dalhousie University, Canada) for sharing genome assemblies of P. magna, P. capuana, P. piriformis and P. parva.
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This work was supported by the Centre National de la Recherche Scientifique (CNRS), Aix-Marseille Université (AMU) and the LABEX Dynamo (ANR-11-LABX-0011-01). Proteomic experiments were partly supported by the Agence Nationale de la Recherche (ANR-10-INBS-08-01 ProFI Grant).
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AA and RvL conceived the study, designed and conducted the experiments. OV, NJT, BL and AA assembled and annotated genomes. YC and SB performed the proteomic studies. AA, RvL, WN and OV performed the bioinformatics analyses. AA, RvL and OV wrote the manuscript and generated the figures. All authors participated and approved the final version of the manuscript.
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van Lis, R., Couté, Y., Brugière, S. et al. Phylogenetic and functional diversity of aldehyde-alcohol dehydrogenases in microalgae. Plant Mol Biol 105, 497–511 (2021). https://doi.org/10.1007/s11103-020-01105-9
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DOI: https://doi.org/10.1007/s11103-020-01105-9