Retrotransposon and CRISPR/Cas9-mediated knockout of NOD26 impairs the legume-rhizobia symbiosis
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Alleva K, Marquez M, Villarreal N, Mut P, Bustamante C, Bellati J, Martínez G, Civello M, Amodeo G (2010) Cloning, functional characterization, and co-expression studies of a novel aquaporin (FaPIP2;1) of strawberry fruit. J Exp Bot 61:3935–3945
Beamer Z, Routray P, Choi W-G, Spangler MK, Lokdarshi A, Roberts DM (2020) The Arabidopsis thaliana NIP2;1 lactic acid channel promotes plant survival under low oxygen stress. Biorxiv 239(7):92
Blumwald E, Fortin MG, Rea PA, Verma DP, Poole RJ (1985) Presence of host-plasma membrane type H-ATPase in the membrane envelope enclosing the bacteroids in soybean root nodules. Plant Physiol 78:665–672
Bottero E, Massa G, González M, Stritzler M, Tajima H, Gómez C, Frare R, Feingold S, Blumwald E, Ayub N, Soto G (2021) Efficient CRISPR/Cas9 genome editing in alfalfa using a public germplasm. Frontiers in Agronomy. https://doi.org/10.3389/fagro.2021.661526
Brambilla S, Soto G, Odorizzi A, Arolfo V, McCormick W, Primo E, Giordano W, Jozefkowicz C, Ayub N (2020) Spontaneous mutations in the nitrate reductase gene napC drive the emergence of eco-friendly low-N2O-emitting alfalfa rhizobia in regions with different climates. Microb Ecol 79:1044–1053
Cai J, Zhang L-Y, Liu W, Tian Y, Xiong J-S, Wang Y-H, Li R-J, Li H-M, Wen J, Mysore KS, Boller T, Xie Z-P, Staehelin C (2018) Role of the nod factor hydrolase MtNFH1 in regulating nod factor levels during rhizobial infection and in mature nodules of Medicago truncatula. Plant Cell 30:397–414
Cermak T, Curtin SJ, Gil-Humanes J, Cegan R, Kono TJY, Konecna E, Belanto JJ, Starker CG, Mathre JW, Greenstein RL, Voytas DF (2017) A multipurpose toolkit to enable advanced genome engineering in plants. Plant Cell 29:1196–1217
Clarke VC, Loughlin PC, Gavrin A, Chen C, Brear EM, Day DA, Smith PM (2015) Proteomic analysis of the soybean symbiosome identifies new symbiotic proteins. Mol Cell Proteomics 14:1301–1322
Conant GC, Wolfe KH (2008) Turning a hobby into a job: how duplicated genes find new functions. Nat Rev Genet 9:938–950
d’Erfurth I, Cosson V, Eschstruth A, Lucas H, Kondorosi A, Ratet P (2003) Efficient transposition of the Tnt1 tobacco retrotransposon in the model legume Medicago truncatula. Plant J 34:95–106
Dean RM, Rivers RL, Zeidel ML, Roberts DM (1999) Purification and functional reconstitution of soybean nodulin 26. An aquaporin with water and glycerol transport properties. Biochemistry 38:347–353
Di Giorgio JAP, Bienert GP, Ayub ND, Yaneff A, Barberini ML, Mecchia MA, Amodeo G, Soto GC, Muschietti JP (2016) Pollen-specific aquaporins NIP4;1 and NIP4;2 are required for pollen development and pollination in Arabidopsis thaliana. Plant Cell 28:1053–1077
diCenzo GC, Tesi M, Pfau T, Mengoni A, Fondi M (2020) Genome-scale metabolic reconstruction of the symbiosis between a leguminous plant and a nitrogen-fixing bacterium. Nat Commun 11:2574
Fortin MG, Morrison NA, Verma DP (1987) Nodulin-26, a peribacteroid membrane nodulin is expressed independently of the development of the peribacteroid compartment. Nucleic Acids Res 15:813–824
Fox AR, Soto G, Valverde C, Russo D, Lagares A Jr, Zorreguieta Á, Alleva K, Pascuan C, Frare R, Mercado-Blanco J, Dixon R, Ayub ND (2016) Major cereal crops benefit from biological nitrogen fixation when inoculated with the nitrogen-fixing bacterium Pseudomonas protegens Pf-5 X940. Environ Microbiol 18:3522–3534
Frare R, Ayub N, Alleva K, Soto G (2018) The ammonium channel NOD26 is the evolutionary innovation that drives the emergence, consolidation, and dissemination of nitrogen-fixing symbiosis in angiosperms. J Mol Evol 86:554–565
Frare R, Stritzler M, Pascuan C, Liebrenz K, Galindo-Sotomonte L, Soto L, Nikel PI, Ayub N (2020) Elimination of GlnKAmtB affects serine biosynthesis and improves growth and stress tolerance of Escherichia coli under nutrient-rich conditions. FEMS Microbiol Lett, Accepted Manuscript. https://doi.org/10.1093/femsle/fnaa1197
Galibert F, Finan TM, Long SR, Batut J (2001) The composite genome of the legume symbiont Sinorhizobium meliloti. Science 293:668–672
García AN, Ayub ND, Fox AR, Gómez MC, Diéguez MJ, Pagano EM, Berini CA, Muschietti JP, Soto G (2014) Alfalfa snakin-1 prevents fungal colonization and probably coevolved with rhizobia. BMC Plant Biol 14:248
Guenther JF, Chanmanivone N, Galetovic MP, Wallace IS, Cobb JA, Roberts DM (2003) Phosphorylation of soybean nodulin 26 on serine 262 enhances water permeability and is regulated developmentally and by osmotic signals. Plant Cell 15:981–991
Hoffmann B, Trinh TH, Leung J, Kondorosi A, Kondorosi E (1997) A new medicago truncatula line with superior in vitro regeneration, transformation, and symbiotic properties isolated through cell culture selection. Mol Plant-Microbe Interact 10:307–315
Hwang JH, Ellingson SR, Roberts DM (2010) Ammonia permeability of the soybean nodulin 26 channel. FEBS Lett 584:4339–4343
Ikaga R, Namekata I, Kotiadis VN, Ogawa H, Duchen MR, Tanaka H, Iida-Tanaka N (2015) Knockdown of aquaporin-8 induces mitochondrial dysfunction in 3T3-L1 cells. Biochem Biophys Rep 4:187–195
Jones KM, Kobayashi H, Davies BW, Taga ME, Walker GC (2007) How rhizobial symbionts invade plants: the Sinorhizobium-Medicago model. Nat Rev Microbiol 5:619–633
Jozefkowicz C, Frare R, Fox R, Odorizzi A, Arolfo V, Pagano E, Basigalup D, Ayub N, Soto G (2018) Maximizing the expression of transgenic traits into elite alfalfa germplasm using a supertransgene configuration in heterozygous conditions. Theor Appl Genet 131:1111–1123
Kelemen Z, Mai A, Kapros T, Feher A, Gyorgyey J, Waterborg JH, Dudits D (2002) Transformation vector based on promoter and intron sequences of a replacement histone H3 gene. A tool for high, constitutive gene expression in plants. Transgenic Res 11:69–72
Loehlin DW, Carroll SB (2016) Expression of tandem gene duplicates is often greater than twofold. Proc Natl Acad Sci 113:5988–5992
Magne K, Couzigou J-M, Schiessl K, Liu S, George J, Zhukov V, Sahl L, Boyer F, Iantcheva A, Mysore KS, Wen J, Citerne S, Oldroyd GED, Ratet P (2018) MtNODULE ROOT1 and MtNODULE ROOT2 are essential for indeterminate nodule identity. Plant Physiol 178:295–316
Masalkar P, Wallace IS, Hwang JH, Roberts DM (2010) Interaction of cytosolic glutamine synthetase of soybean root nodules with the C-terminal domain of the symbiosome membrane nodulin 26 aquaglyceroporin. J Biol Chem 285:23880–23888
Mergaert P, Kereszt A, Kondorosi E (2020) Gene expression in nitrogen-fixing symbiotic nodule cells in Medicago truncatula and other nodulating plants. Plant Cell 32:42–68
Molinas SM, Trumper L, Marinelli RA (2012) Mitochondrial aquaporin-8 in renal proximal tubule cells: evidence for a role in the response to metabolic acidosis. Am J Physiol Renal Physiol 303:F458-466
Nagymihály M, Veluchamy A, Györgypál Z, Ariel F, Jégu T, Benhamed M, Szűcs A, Kereszt A, Mergaert P, Kondorosi É (2017) Ploidy-dependent changes in the epigenome of symbiotic cells correlate with specific patterns of gene expression. Proc Natl Acad Sci USA 114:4543–4548
Niemietz CM, Tyerman SD (2000) Channel-mediated permeation of ammonia gas through the peribacteroid membrane of soybean nodules. FEBS Lett 465:110–114
Panchy N, Lehti-Shiu M, Shiu S-H (2016) Evolution of gene duplication in plants. Plant Physiol 171:2294–2316
Pascuan C, Bottero E, Kapros T, Ayub N, Soto G (2020) pBAR–H3.2, a native-optimized binary vector to bypass transgene silencing in alfalfa. Plant Cell Rep 39:683–685
Perez Di Giorgio J, Soto G, Alleva K, Jozefkowicz C, Amodeo G, Muschietti JP, Ayub ND (2014) Prediction of aquaporin function by integrating evolutionary and functional analyses. J Membr Biol 247:107–125
Pierre O, Engler G, Hokins J, Brau F, Boncompagni E, Herouart D (2013) Peribacteroid space acidification: a marker of mature bacteroid functioning in Medicago truncatula nodules. Plant Cell Environ 36:2059–2070
Pislariu CI, Sinharoy S, Torres-Jerez I, Nakashima J, Blancaflor EB, Udvardi MK (2019) The nodule-specific PLAT domain protein NPD1 is required for nitrogen-fixing symbiosis. Plant Physiol 180:1480–1497
Rivers RL, Dean RM, Chandy G, Hall JE, Roberts DM, Zeidel ML (1997) Functional analysis of nodulin 26, an aquaporin in soybean root nodule symbiosomes. J Biol Chem 272:16256–16261
Routray P, Masalkar PD, Roberts DM (2015) Nodulin intrinsic proteins: facilitators of water and ammonia transport across the symbiosome membrane. In: de Bruijn FJ (ed) Biological nitrogen fixation. John Wiley & Sons Inc, NJ, pp 695–704
Roux B, Rodde N, Jardinaud MF, Timmers T, Sauviac L, Cottret L, Carrère S, Sallet E, Courcelle E, Moreau S, Debellé F, Capela D, de Carvalho-Niebel F, Gouzy J, Bruand C, Gamas P (2014) An integrated analysis of plant and bacterial gene expression in symbiotic root nodules using laser-capture microdissection coupled to RNA sequencing. Plant J 77:817–837
Setten L, Soto G, Mozzicafreddo M, Fox AR, Lisi C, Cuccioloni M, Angeletti M, Pagano E, Diaz-Paleo A, Ayub ND (2013) Engineering Pseudomonas protegens Pf-5 for nitrogen fixation and its application to improve plant growth under nitrogen-deficient conditions. PLoS ONE 8:e63666
Soria LR, Fanelli E, Altamura N, Svelto M, Marinelli RA, Calamita G (2010) Aquaporin-8-facilitated mitochondrial ammonia transport. Biochem Biophys Res Commun 393:217–221
Soto G, Alleva K, Mazzella MA, Amodeo G, Muschietti JP (2008) AtTIP1;3 and AtTIP5;1, the only highly expressed Arabidopsis pollen-specific aquaporins, transport water and urea. FEBS Lett 582:4077–4082
Soto G, Fox R, Ayub N, Alleva K, Guaimas F, Erijman EJ, Mazzella A, Amodeo G, Muschietti J (2010) TIP5;1 is an aquaporin specifically targeted to pollen mitochondria and is probably involved in nitrogen remobilization in Arabidopsis thaliana. Plant J 64:1038–1047
Tadege M, Wen J, He J, Tu H, Kwak Y, Eschstruth A, Cayrel A, Endre G, Zhao PX, Chabaud M, Ratet P, Mysore KS (2008) Large-scale insertional mutagenesis using the Tnt1 retrotransposon in the model legume Medicago truncatula. Plant J 54:335–347
Torres-Dorante L, Paredes-Melesio R, Link A, Lammel J (2016) A methodology to develop algorithms that predict nitrogen fertilizer needs in maize based on chlorophyll measurements: a case study in Central Mexico. J Agric Sci 154:705–719