Abstract
Carbonic anhydrases (CAs), as zinc metalloenzymes, are ubiquitous in nature and play essential roles in diverse biological processes. Although CAs have been broadly explored and studied, comprehensive characteristics of CA gene family members in the soybean (Glycine max) are still lacking. A total of 35 CA genes (GmCAs) were identified; they distributed on sixteen chromosomes of the soybean genome and can be divided into three subfamilies (α-type, β-type, and γ-type). Bioinformatics analysis showed that the specific GmCA gene subfamily or clade exhibited similar characteristics and that segmental duplications took the major role in generating new GmCAs. Furthermore, the synteny and evolutionary constraints analyses of CAs among soybean and distinct species provided more detailed evidence for GmCA gene family evolution. Cis-element analysis of promoter indicated that GmCAs may be responsive to abiotic stress and regulate photosynthesis. Moreover, the expression patterns of GmCAs varied in different tissues at diverse developmental stages in soybean. Additionally, we found that eight representative GmCAs may be involved in the response of soybean to low phosphorus stress. The systematic investigation of the GmCA gene family in this study will provide a valuable basis for further functional research on soybean CA genes.
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Data Availability
RNA-seq data used in this study are available in the National Center for Biotechnology Information Sequence Read Archive (SRA) under the BioProject accession number of PRJNA741780. All data described in the study have been provided in the Supplementary Information.
References
Blanco-Rivero A, Shutova T, Román M, Villarejo A, Martinez F (2012) Phosphorylation controls the localization and activation of the lumenal carbonic anhydrase in Chlamydomonas reinhardtii. PLoS One 7(11):e49063. https://doi.org/10.1371/journal.pone.0049063
Burén S, Ortega-Villasante C, Blanco-Rivero A, Martínez-Bernardini A, Shutova T, Shevela D, Messinger J, Bako L, Villarejo A, Samuelsson G (2011) Importance of post-translational modifications for functionality of a chloroplast-localized carbonic anhydrase (CAH1) in Arabidopsis thaliana. PLoS One 6(6):e21021. https://doi.org/10.1371/journal.pone.0021021
Cannon S, Mitra A, Baumgarten A, Young N, May G (2004) The roles of segmental and tandem gene duplication in the evolution of large gene families in Arabidopsis thaliana. BMC Plant Biol 4:10. https://doi.org/10.1186/1471-2229-4-10
Chen C, Chen H, Zhang Y, Thomas H, Frank M, He Y, Xia R (2020) TBtools: an integrative toolkit developed for interactive analyses of big biological data. Mol Plant 13(8):1194–1202. https://doi.org/10.1016/j.molp.2020.06.009
Chou K-C, Shen H-B (2008) Cell-PLoc 2.0: an improved package of web-servers for predicting subcellular localization of proteins in various organisms. Nat Protoc 3(2):153–162. https://doi.org/10.1038/nprot.2007.494
Clayton H, Saladié M, Rolland V, Sharwood R, Macfarlane T, Ludwig M (2017) Loss of the chloroplast transit peptide from an ancestral C3 carbonic anhydrase is associated with C4 evolution in the grass genus Neurachne. Plant Physiol 173(3):1648–1658. https://doi.org/10.1104/pp.16.01893
Cong W, Suriyagoda L, Lambers H (2020) Tightening the phosphorus cycle through phosphorus-efficient crop genotypes. Trends Plant Sci 25(10):967–975. https://doi.org/10.1016/j.tplants.2020.04.013
Dąbrowska-Bronk J, Komar D, Rusaczonek A, Kozłowska-Makulska A, Szechyńska-Hebda M, Karpiński S (2016) β-carbonic anhydrases and carbonic ions uptake positively influence Arabidopsis photosynthesis, oxidative stress tolerance and growth in light dependent manner. J Plant Physiol 203:44–54. https://doi.org/10.1016/j.jplph.2016.05.013
DiMario RJ, Quebedeaux JC, Longstreth DJ, Dassanayake M, Hartman MM, Moroney JV (2016) The cytoplasmic carbonic anhydrases β CA2 and β CA4 are required for optimal plant growth at low CO2. Plant Physiol 171(1):280–293. https://doi.org/10.1104/pp.15.01990
DiMario R, Clayton H, Mukherjee A, Ludwig M, Moroney J (2017) Plant carbonic anhydrases: structures, locations, evolution, and physiological roles. Mol Plant 10(1):30–46. https://doi.org/10.1016/j.molp.2016.09.001
Duvaud S, Gabella C, Lisacek F, Stockinger H, Ioannidis V, Durinx C (2021) Expasy, the Swiss Bioinformatics Resource Portal, as designed by its users. Nucleic Acids Res 49:W216–W227. https://doi.org/10.1093/nar/gkab225
Everson R (1970) Carbonic anhydrase and CO2 fixation in isolated chloroplasts. Phytochemistry 9(1):25–32. https://doi.org/10.1016/S0031-9422(00)86610-8
Fabre N, Reiter I, Becuwe-Linka N, Genty B, Rumeau D (2007) Characterization and expression analysis of genes encoding alpha and beta carbonic anhydrases in Arabidopsis. Plant Cell Environ 30(5):617–629. https://doi.org/10.1111/j.1365-3040.2007.01651.x
Feng C-Y, Chen Z-F, Pei L-L, Ma S-X, Nie H-M, Zheng S-W, Sun S, Xing G-M (2020) Genome-wide identification, phylogeny, and expression analysis of the CA gene family in tomato. Biotechnol Biotechnol Equip 34(1):70–83. https://doi.org/10.1016/j.gene.2015.07.055
Finn R, Clements J, Eddy S (2011) HMMER web server: interactive sequence similarity searching. Nucleic Acids Res 39:W29–W37. https://doi.org/10.1093/nar/gkr367
Floryszak-Wieczorek J, Arasimowicz-Jelonek M (2017) The multifunctional face of plant carbonic anhydrase. Plant Physiol Biochem 112:362–368. https://doi.org/10.1016/j.plaphy.2017.01.007
Hatch MD, Burnell JN (1990) Carbonic anhydrase activity in leaves and its role in the first step of C4 photosynthesis. Plant Physiol 93(2):825–828. https://doi.org/10.1104/pp.93.2.825
Hewett-Emmett D, Tashian RE (1996) Functional diversity, conservation, and convergence in the evolution of the α-, β-, and γ-carbonic anhydrase gene families. Mol Phylogenet Evol 5(1):50–77. https://doi.org/10.1006/mpev.1996.0006
Hoang C, Chapman K (2002) Biochemical and molecular inhibition of plastidial carbonic anhydrase reduces the incorporation of acetate into lipids in cotton embryos and tobacco cell suspensions and leaves. Plant Physiol 128(4):1417–1427. https://doi.org/10.1104/pp.010879
Hossain Z, Makino T, Komatsu S (2012) Proteomic study of β-aminobutyric acid-mediated cadmium stress alleviation in soybean. J Proteomics 75(13):4151–4164. https://doi.org/10.1016/j.jprot.2012.05.037
Hu H, Boisson-Dernier A, Israelsson-Nordström M, Böhmer M, Xue S, Ries A, Godoski J, Kuhn J, Schroeder J (2010) Carbonic anhydrases are upstream regulators of CO2-controlled stomatal movements in guard cells. Nat Cell Biol 12(1):87–93. https://doi.org/10.1038/ncb2009
Hu H, Rappel W, Occhipinti R, Ries A, Böhmer M, You L, Xiao C, Engineer C, Boron W, Schroeder J (2015) Distinct cellular locations of carbonic anhydrases mediate carbon dioxide control of stomatal movements. Plant Physiol 169(2):1168–1178. https://doi.org/10.1104/pp.15.00646
Hurst L (2002) The Ka/Ks ratio: diagnosing the form of sequence evolution. Trends Genet 18(9):486. https://doi.org/10.1016/s0168-9525(02)02722-1
Iwamoto M, Maekawa M, Saito A, Higo H, Higo K (1998) Evolutionary relationship of plant catalase genes inferred from exon-intron structures: isozyme divergence after the separation of monocots and dicots. Theor Appl Genet 97(1):9–19. https://doi.org/10.1007/s001220050861
Jiang C, Tholen D, Xu JM, Xin C, Zhang H, Zhu X, Zhao Y (2014) Increased expression of mitochondria-localized carbonic anhydrase activity resulted in an increased biomass accumulation in Arabidopsis thaliana. J Plant Biol 57(6):366–374. https://doi.org/10.1007/s12374-014-0330-8
Kavroulakis N, Flemetakis E, Aivalakis G, Dahiya P, Brewin NJ, Fasseas K, Hatzopoulos P, Katinakis P (2003) Tissue distribution and subcellular localization of carbonic anhydrase in mature soybean root nodules indicates a role in CO2 diffusion. Plant Physiol Biochem 41(5):479–484. https://doi.org/10.1016/s0981-9428(03)00056-1
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2− ΔΔCT method. Methods 25(4):402–408. https://doi.org/10.1006/meth.2001.1262
Makita Y, Shimada S, Kawashima M, Kondou-Kuriyama T, Toyoda T, Matsui M (2015) MOROKOSHI: transcriptome database in Sorghum bicolor. Plant Cell Physiol 56(1):e6. https://doi.org/10.1093/pcp/pcu187
Moroney J, Bartlett S, Samuelsson G (2001) Carbonic anhydrases in plants and algae. Plant Cell Environ 24(2):141–153. https://doi.org/10.1111/j.1365-3040.2001.00669.x
Moroney JV, Ma Y, Frey WD, Fusilier KA, Pham TT, Simms TA, DiMario RJ, Yang J, Mukherjee B (2011) The carbonic anhydrase isoforms of Chlamydomonas reinhardtii: intracellular location, expression, and physiological roles. Photosyn Res 109(1):133–149. https://doi.org/10.1007/s11120-011-9635-3
Navarro A, Barton N (2003) Chromosomal speciation and molecular divergence--accelerated evolution in rearranged chromosomes. Science 300(5617):321–324. https://doi.org/10.1126/science.1080600
Ohki K (1978) Zinc Concentration in Soybean as Related to Growth, Photosynthesis, and Carbonic Anhydrase Activity. Crop Sci 18(1):79. https://doi.org/10.2135/cropsci1978.0011183x001800010021x
Roy SW, Penny D (2007) A very high fraction of unique intron positions in the intron-rich diatom Thalassiosira pseudonana indicates widespread intron gain. Mol Biol Evol 24(7):1447–1457. https://doi.org/10.1093/molbev/msm048
Rudenko N, Ignatova L, Fedorchuk T, Ivanov B (2015) Carbonic anhydrases in photosynthetic cells of higher plants. Biochemistry 80(6):674–687. https://doi.org/10.1134/S0006297915060048
Schmitz R, Grotewold E, Stam M (2022) Cis-regulatory sequences in plants: their importance, discovery, and future challenges. Plant Cell 34(2):718–741. https://doi.org/10.1093/plcell/koab281
Schmutz J, Cannon SB, Schlueter J, Ma J, Mitros T, Nelson W, Hyten DL, Song Q, Thelen JJ, Cheng J (2010) Genome sequence of the palaeopolyploid soybean. Nature 463(7278):178–183. https://doi.org/10.1038/nature08670
Severin AJ, Woody JL, Bolon Y-T, Joseph B, Diers BW, Farmer AD, Muehlbauer GJ, Nelson RT, Grant D, Specht JE (2010) RNA-Seq Atlas of Glycine max: a guide to the soybean transcriptome. BMC Plant Biol 10(1):1–16. https://doi.org/10.1186/1471-2229-10-160
Shoemaker R, Schlueter J, Doyle J (2006) Paleopolyploidy and gene duplication in soybean and other legumes. Curr Opin Plant Biol 9(2):104–109. https://doi.org/10.1016/j.pbi.2006.01.007
Smith K, Ferry J (2000) Prokaryotic carbonic anhydrases. FEMS Microbiol Rev 24(4):335–366. https://doi.org/10.1111/j.1574-6976.2000.tb00546.x
Soto D, Córdoba JP, Villarreal F, Bartoli C, Schmitz J, Maurino VG, Braun HP, Pagnussat GC, Zabaleta E (2015) Functional characterization of mutants affected in the carbonic anhydrase domain of the respiratory complex I in Arabidopsis thaliana. Plant J 83(5):831–844. https://doi.org/10.1111/tpj.12930
Studer A, Gandin A, Kolbe A, Wang L, Cousins A, Brutnell T (2014) A limited role for carbonic anhydrase in C4 photosynthesis as revealed by a ca1ca2 double mutant in maize. Plant Physiol 165(2):608–617. https://doi.org/10.1104/pp.114.237602
Sunderhaus S, Dudkina NV, Jänsch L, Klodmann J, Heinemeyer J, Perales M, Zabaleta E, Boekema EJ, Braun H-P (2006) Carbonic anhydrase subunits form a matrix-exposed domain attached to the membrane arm of mitochondrial complex I in plants. J Biol Chem 281(10):6482–6488. https://doi.org/10.1074/jbc.M511542200
Tang H, Krishnakumar V, Bidwell S, Rosen B, Chan A, Zhou S, Gentzbittel L, Childs K, Yandell M, Gundlach H, Mayer K, Schwartz D, Town C (2014) An improved genome release (version Mt4.0) for the model legume Medicago truncatula. BMC Genom 15:312. https://doi.org/10.1186/1471-2164-15-312
Tanz SK, Tetu SG, Vella NG, Ludwig M (2009) Loss of the transit peptide and an increase in gene expression of an ancestral chloroplastic carbonic anhydrase were instrumental in the evolution of the cytosolic C4 carbonic anhydrase in Flaveria. Plant Physiol 150(3):1515–1529. https://doi.org/10.1104/pp.109.137513
Tetu SG, Tanz SK, Vella N, Burnell JN, Ludwig M (2007) The Flaveria bidentis β-carbonic anhydrase gene family encodes cytosolic and chloroplastic isoforms demonstrating distinct organ-specific expression patterns. Plant Physiol 144(3):1316–1327. https://doi.org/10.1104/pp.107.098152
Tiwari A, Kumar P, Singh S, Ansari S (2005) Carbonic anhydrase in relation to higher plants. Photosynthetica 43(1):1–11. https://doi.org/10.1007/s11099-005-1011-0
Villarejo A, Burén S, Larsson S, Déjardin A, Monné M, Rudhe C, Karlsson J, Jansson S, Lerouge P, Rolland N (2005) Evidence for a protein transported through the secretory pathway en route to the higher plant chloroplast. Nat Cell Biol 7(12):1224–1231. https://doi.org/10.1038/ncb1330
Wang Z, Gerstein M, Snyder M (2009) RNA-Seq: a revolutionary tool for transcriptomics. Nat Rev Genet 10(1):57–63. https://doi.org/10.1038/nrg2484
Wang M, Zhang Q, Liu F, Xie W, Wang G, Wang J, Gao Q, Duan K (2014) Family-wide expression characterization of Arabidopsis beta-carbonic anhydrase genes using qRT-PCR and Promoter::GUS fusions. Biochimie 97:219–227. https://doi.org/10.1016/j.biochi.2013.10.020
Wang L, Liang J, Zhou Y, Tian T, Zhang B, Duanmu D (2021) Molecular characterization of carbonic anhydrase genes in Lotus japonicus and their potential roles in symbiotic nitrogen fixation. Int J Mol Sci 22(15):7766. https://doi.org/10.3390/ijms22157766
William Roy S, Gilbert W (2006) The evolution of spliceosomal introns: patterns, puzzles and progress. Nat Rev Genet 7(3):211–221. https://doi.org/10.1038/nrg1807
Xie T, Chen C, Li C, Liu J, Liu C, He Y (2018) Genome-wide investigation of WRKY gene family in pineapple: evolution and expression profiles during development and stress. BMC Genom 19(1):490. https://doi.org/10.1186/s12864-018-4880-x
Yang F, Xu X, Wang W, Ma J, Wei D, He P, Pampolino M, Johnston A (2017) Estimating nutrient uptake requirements for soybean using QUEFTS model in China. PLoS One 12(5):e0177509. https://doi.org/10.1371/journal.pone.0177509
Yang Y, Zhu X, Cui R, Wang R, Li H, Wang J, Chen H, Zhang D (2021) Identification of soybean phosphorous efficiency QTLs and genes using chlorophyll fluorescence parameters through GWAS and RNA-seq. Planta 254(6):1–13. https://doi.org/10.1007/s00425-021-03760-8
Zhu Y, Wu N, Song W, Yin G, Qin Y, Yan Y, Hu Y (2014) Soybean (Glycine max) expansin gene superfamily origins: segmental and tandem duplication events followed by divergent selection among subfamilies. BMC Plant Biol 14:93. https://doi.org/10.1186/1471-2229-14-93
Ignatova L, Rudenko N, Zhurikova E, Borisova-Mubarakshina M, Ivanov B (2019) Carbonic anhydrases in photosynthesizing cells of C3 higher plants. Metabolites 9(4). https://doi.org/10.3390/metabo9040073
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The work was supported in part by the National Natural Science Foundation of China (32072088, 32272171, and 32201867), Major Science and Technology Project of Henan Province (221100110300) and Henan Fine Variety Joint Tackling Key Problems Project (20220100304), and the Central Plains Talents Program Top Young Talents.
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DZ and YMY conceived and designed the research. LW conducted the data analysis, experiments, and finished the original manuscript. RYW, RFC, and HQZ carried out the RT-qPCR experiment. LW wrote the manuscript. YMY, JYZ, ZWH, and DZ revised the manuscript. All authors discussed the results and contributed to the manuscript.
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Wang, L., Zhang, J., Wang, R. et al. Genome-wide identification, evolution, and expression analysis of carbonic anhydrases genes in soybean (Glycine max). Funct Integr Genomics 23, 37 (2023). https://doi.org/10.1007/s10142-023-00966-9
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DOI: https://doi.org/10.1007/s10142-023-00966-9