An extracellular β-N-acetylhexosaminidase of Medicago truncatula hydrolyzes chitooligosaccharides and is involved in arbuscular mycorrhizal symbiosis but not required for nodulation.
Medicago truncatula
N-acetylglucosamine
arbuscular mycorrhizal symbiosis
chitooligosaccharides
glycoside hydrolase
β-N-acetylhexosaminidase
Journal
The New phytologist
ISSN: 1469-8137
Titre abrégé: New Phytol
Pays: England
ID NLM: 9882884
Informations de publication
Date de publication:
09 2023
09 2023
Historique:
received:
27
02
2023
accepted:
18
05
2023
medline:
3
8
2023
pubmed:
7
7
2023
entrez:
7
7
2023
Statut:
ppublish
Résumé
Establishment of symbiosis between plants and arbuscular mycorrhizal (AM) fungi depends on fungal chitooligosaccharides (COs) and lipo-chitooligosaccharides (LCOs). The latter are also produced by nitrogen-fixing rhizobia to induce nodules on leguminous roots. However, host enzymes regulating structure and levels of these signals remain largely unknown. Here, we analyzed the expression of a β-N-acetylhexosaminidase gene of Medicago truncatula (MtHEXO2) and biochemically characterized the enzyme. Mutant analysis was performed to study the role of MtHEXO2 during symbiosis. We found that expression of MtHEXO2 is associated with AM symbiosis and nodulation. MtHEXO2 expression in the rhizodermis was upregulated in response to applied chitotetraose, chitoheptaose, and LCOs. M. truncatula mutants deficient in symbiotic signaling did not show induction of MtHEXO2. Subcellular localization analysis indicated that MtHEXO2 is an extracellular protein. Biochemical analysis showed that recombinant MtHEXO2 does not cleave LCOs but can degrade COs into N-acetylglucosamine (GlcNAc). Hexo2 mutants exhibited reduced colonization by AM fungi; however, nodulation was not affected in hexo2 mutants. In conclusion, we identified an enzyme, which inactivates COs and promotes the AM symbiosis. We hypothesize that GlcNAc produced by MtHEXO2 may function as a secondary symbiotic signal.
Substances chimiques
oligochitosan
0
beta-N-Acetylhexosaminidases
EC 3.2.1.52
Chitin
1398-61-4
Plant Proteins
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
1954-1973Informations de copyright
© 2023 The Authors. New Phytologist © 2023 New Phytologist Foundation.
Références
Afkhami ME, Stinchcombe JR. 2016. Multiple mutualist effects on genome-wide expression in the tripartite association between Medicago truncatula, nitrogen-fixing bacteria and mycorrhizal fungi. Molecular Ecology 25: 4946-4962.
Alvisi N, van Noort K, Dwiani S, Geschiere N, Sukarta O, Varossieau K, Nguyen DL, Strasser R, Hokke CH, Schots A et al. 2021. β-Hexosaminidases along the secretory pathway of Nicotiana benthamiana have distinct specificities toward engineered helminth N-glycans on recombinant glycoproteins. Frontiers in Plant Science 12: 638454.
Benedito VA, Torres-Jerez I, Murray JD, Andriankaja A, Allen S, Kakar K, Wandrey M, Verdier J, Zuber H, Ott T et al. 2008. A gene expression atlas of the model legume Medicago truncatula. The Plant Journal 55: 504-513.
Boisson-Dernier A, Chabaud M, Garcia F, Bécard G, Rosenberg C, Barker DG. 2001. Agrobacterium rhizogenes-transformed roots of Medicago truncatula for the study of nitrogen-fixing and endomycorrhizal symbiotic associations. Molecular Plant-Microbe Interactions 14: 695-700.
Bonfante-Fasolo P, Faccio A, Perotto S, Schubert A. 1990. Correlation between chitin distribution and cell wall morphology in the mycorrhizal fungus Glomus versiforme. Mycological Research 94: 157-165.
Boulanger A, Zischek C, Lautier M, Jamet S, Rival P, Carrere S, Arlat M, Lauber E. 2014. The plant pathogen Xanthomonas campestris pv. campestris exploits N-acetylglucosamine during infection. mBio 5: e01527-14.
Bozsoki Z, Cheng J, Feng F, Gysel K, Vinther M, Andersen KR, Oldroyd G, Blaise M, Radutoiu S, Stougaard J. 2017. Receptor-mediated chitin perception in legume roots is functionally separable from Nod factor perception. Proceedings of the National Academy of Sciences, USA 114: E8118-E8127.
Bozsoki Z, Gysel K, Hansen SB, Lironi D, Krönauer C, Feng F, de Jong N, Vinther M, Kamble M, Thygesen MB et al. 2020. Ligand-recognizing motifs in plant LysM receptors are major determinants of specificity. Science 369: 663-670.
Breakspear A, Liu C, Roy S, Stacey N, Rogers C, Trick M, Morieri G, Mysore KS, Wen J, Oldroyd GED et al. 2014. The root hair “infectome” of Medicago truncatula uncovers changes in cell cycle genes and reveals a requirement for auxin signaling in rhizobial infection. Plant Cell 26: 4680-4701.
Broghammer A, Krusell L, Blaise M, Sauer J, Sullivan JT, Maolanon N, Vinther M, Lorentzen A, Madsen EB, Jensen KJ et al. 2012. Legume receptors perceive the rhizobial lipochitin oligosaccharide signal molecules by direct binding. Proceedings of the National Academy of Sciences, USA 109: 13859-13864.
Cai J, Zhang LY, Liu W, Tian Y, Xiong JS, Wang YH, Li RJ, Li HM, Wen JQ, Mysore KS et al. 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.
Capoen W, Sun J, Wysham D, Otegui MS, Venkateshwaran M, Hirsch S, Miwa H, Downie JA, Morris RJ, Ané J-M et al. 2011. Nuclear membranes control symbiotic calcium signaling of legumes. Proceedings of the National Academy of Sciences, USA 108: 14348-14353.
Carrere S, Verdier J, Gamas P. 2021. MtExpress, a comprehensive and curated RNAseq-based gene expression atlas for the model legume Medicago truncatula. Plant and Cell Physiology 62: 1494-1500.
Castilho A, Windwarder M, Gattinger P, Mach L, Strasser R, Altmann F, Steinkellner H. 2014. Proteolytic and N-glycan processing of human α1-antitrypsin expressed in Nicotiana benthamiana. Plant Physiology 166: 1839-1851.
Catoira R, Galera C, de Billy F, Penmetsa RV, Journet EP, Maillet F, Rosenberg C, Cook D, Gough C, Dénarié J. 2000. Four genes of Medicago truncatula controlling components of a Nod factor transduction pathway. Plant Cell 12: 1647-1666.
Chabaud M, Boisson-Dernier A, Zhang J, Taylor CG, Yu O, Barker DG. 2006a. Agrobacterium rhizogenes-mediated root transformation. In: Mathesius U, Journet EP, Sumner LW, eds. Medicago truncatula handbook. Ardmore, OK, USA: Noble Research Institute.
Chabaud M, Harrison M, de Carvalho-Niebel F, B'ecard G, Barker DG. 2006b. Inoculation and growth with mycorrhizal fungi. In: Mathesius U, Journet EP, Sumner LW, eds. Medicago truncatula handbook. Ardmore, OK, USA: Noble Research Institute.
Chen S, Songkumarn P, Liu J, Wang GL. 2009. A versatile zero background T-vector system for gene cloning and functional genomics. Plant Physiology 150: 1111-1121.
Crosino A, Genre A. 2022. Peace talks: symbiotic signaling molecules in arbuscular mycorrhizas and their potential application. Journal of Plant Interactions 17: 824-839.
Damiani I, Drain A, Guichard M, Balzergue S, Boscari A, Boyer JC, Brunaud V, Cottaz S, Rancurel C, Da Rocha M et al. 2016. Nod factor effects on root hair-specific transcriptome of Medicago truncatula: focus on plasma membrane transport systems and reactive oxygen species networks. Frontiers in Plant Science 7: 794.
Drula E, Garron ML, Dogan S, Lombard V, Henrissat B, Terrapon N. 2022. The carbohydrate-active enzyme database: functions and literature. Nucleic Acids Research 50: D571-D577.
Ehrhardt DW, Wais R, Long SR. 1996. Calcium spiking in plant root hairs responding to rhizobium nodulation signals. Cell 85: 673-681.
Elfstrand M, Feddermann N, Ineichen K, Nagaraj VJ, Wiemken A, Boller T, Salzer P. 2005. Ectopic expression of the mycorrhiza-specific chitinase gene Mtchit 3-3 in Medicago truncatula root-organ cultures stimulates spore germination of glomalean fungi. New Phytologist 167: 557-570.
Fahraeus G. 1957. The infection of clover root hairs by nodule bacteria studied by a simple glass slide technique. Journal of General Microbiology 16: 374-381.
Feng F, Sun J, Radhakrishnan GV, Lee T, Bozsoki Z, Fort S, Gavrin A, Gysel K, Thygesen MB, Andersen KR et al. 2019. A combination of chitooligosaccharide and lipochitooligosaccharide recognition promotes arbuscular mycorrhizal associations in Medicago truncatula. Nature Communications 10: 5047.
Fernández I, Cosme M, Stringlis IA, Yu K, de Jonge R, van Wees SCM, Pozo MJ, Pieterse CMJ, van der Heijden MGA. 2019. Molecular dialogue between arbuscular mycorrhizal fungi and the nonhost plant Arabidopsis thaliana switches from initial detection to antagonism. New Phytologist 223: 867-881.
Fiorilli V, Vallino M, Biselli C, Faccio A, Bagnaresi P, Bonfante P. 2015. Host and non-host roots in rice: cellular and molecular approaches reveal differential responses to arbuscular mycorrhizal fungi. Frontiers in Plant Science 6: 636.
Fournier J, Teillet A, Chabaud M, Ivanov S, Genre A, Limpens E, de Carvalho-Niebel F, Barker DG. 2015. Remodeling of the infection chamber before infection thread formation reveals a two-step mechanism for rhizobial entry into the host legume root hair. Plant Physiology 167: 1233-1242.
Gaude N, Bortfeld S, Duensing N, Lohse M, Krajinski F. 2012. Arbuscule-containing and non-colonized cortical cells of mycorrhizal roots undergo extensive and specific reprogramming during arbuscular mycorrhizal development. The Plant Journal 69: 510-528.
Genre A, Chabaud M, Balzergue C, Puech-Pages V, Novero M, Rey T, Fournier J, Rochange S, Becard G, Bonfante P et al. 2013. Short-chain chitin oligomers from arbuscular mycorrhizal fungi trigger nuclear Ca2+ spiking in Medicago truncatula roots and their production is enhanced by strigolactone. New Phytologist 198: 190-202.
Genre A, Russo G. 2016. Does a common pathway transduce symbiotic signals in plant-microbe interactions? Frontiers in Plant Science 7: 96.
Gibelin-Viala C, Amblard E, Puech-Pages V, Bonhomme M, Garcia M, Bascaules-Bedin A, Fliegmann J, Wen J, Mysore KS, Signor C et al. 2019. The Medicago truncatula LysM receptor-like kinase LYK9 plays a dual role in immunity and the arbuscular mycorrhizal symbiosis. New Phytologist 223: 1516-1529.
Giovannetti M, Mosse B. 1980. An evaluation of techniques for measuring vesicular arbuscular mycorrhizal infection in roots. New Phytologist 84: 489-500.
Girardin A, Wang T, Ding Y, Keller J, Buendia L, Gaston M, Ribeyre C, Gasciolli V, Auriac MC, Vernié T et al. 2019. LCO receptors involved in arbuscular mycorrhiza are functional for rhizobia perception in legumes. Current Biology 29: 4249-4259.
Gomez SK, Javot H, Deewatthanawong P, Torres-Jerez I, Tang Y, Blancaflor EB, Udvardi MK, Harrison MJ. 2009. Medicago truncatula and Glomus intraradices gene expression in cortical cells harboring arbuscules in the arbuscular mycorrhizal symbiosis. BMC Plant Biology 9: 10.
Goormachtig S, Lievens S, Van de Velde W, Van Montagu M, Holsters M. 1998. Srchi13, a novel early nodulin from Sesbania rostrata, is related to acidic class III chitinases. Plant Cell 10: 905-915.
Gutjahr C, Sawers RJ, Marti G, Andres-Hernandez L, Yang SY, Casieri L, Angliker H, Oakeley EJ, Wolfender JL, Abreu-Goodger C et al. 2015. Transcriptome diversity among rice root types during asymbiosis and interaction with arbuscular mycorrhizal fungi. Proceedings of the National Academy of Sciences, USA 112: 6754-6759.
Gutternigg M, Kretschmer-Lubich D, Paschinger K, Rendic D, Hader J, Geier P, Ranftl R, Jantsch V, Lochnit G, Wilson IB. 2007. Biosynthesis of truncated N-linked oligosaccharides results from non-orthologous hexosaminidase-mediated mechanisms in nematodes, plants, and insects. The Journal of Biological Chemistry 282: 27825-27840.
He J, Zhang C, Dai H, Liu H, Zhang X, Yang J, Chen X, Zhu Y, Wang D, Qi X et al. 2019. A LysM receptor heteromer mediates perception of arbuscular mycorrhizal symbiotic signal in rice. Molecular Plant 12: 1561-1576.
Heidstra R, Geurts R, Franssen H, Spaink HP, Van Kammen A, Bisseling T. 1994. Root hair deformation activity of nodulation factors and their fate on Vicia sativa. Plant Physiology 105: 787-797.
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. Molecular Plant-Microbe Interactions 10: 307-315.
Hood EE, Gelvin SB, Melchers LS, Hoekema A. 1993. New Agrobacterium helper plasmids for gene transfer to plants. Transgenic Research 2: 208-218.
Hooykaas MJG, Hooykaas PJJ. 2021. The genome sequence of hairy root Rhizobium rhizogenes strain LBA9402: bioinformatics analysis suggests the presence of a new opine system in the agropine Ri plasmid. MicrobiologyOpen 10: e1180.
Hou Y, Vocadlo DJ, Leung A, Withers SG, Mahuran D. 2001. Characterization of the Glu and Asp residues in the active site of human β-hexosaminidase B. Biochemistry 40: 2201-2209.
Jardinaud MF, Boivin S, Rodde N, Catrice O, Kisiala A, Lepage A, Moreau S, Roux B, Cottret L, Sallet E et al. 2016. A laser dissection-RNAseq analysis highlights the activation of cytokinin pathways by Nod factors in the Medicago truncatula root epidermis. Plant Physiology 171: 2256-2276.
Khokhani D, Carrera Carriel C, Vayla S, Irving TB, Stonoha-Arther C, Keller NP, Ané JM. 2021. Deciphering the chitin code in plant symbiosis, defense, and microbial networks. Annual Review of Microbiology 75: 583-607.
Kobae Y, Kawachi M, Saito K, Kikuchi Y, Ezawa T, Maeshima M, Hata S, Fujiwara T. 2015. Up-regulation of genes involved in N-acetylglucosamine uptake and metabolism suggests a recycling mode of chitin in intraradical mycelium of arbuscular mycorrhizal fungi. Mycorrhiza 25: 411-417.
Lefebvre B, Klaus-Heisen D, Pietraszewska-Bogiel A, Herve C, Camut S, Auriac MC, Gasciolli V, Nurisso A, Gadella TW, Cullimore J. 2012. Role of N-glycosylation sites and CXC motifs in trafficking of Medicago truncatula Nod factor perception protein to plasma membrane. The Journal of Biological Chemistry 287: 10812-10823.
Lever M. 1972. A new reaction for colorimetric determination of carbohydrates. Analytical Biochemistry 47: 273-279.
Lévy J, Bres C, Geurts R, Chalhoub B, Kulikova O, Duc G, Journet EP, Ané J, Lauber E, Bisseling T et al. 2004. A putative Ca2+ and calmodulin-dependent protein kinase required for bacterial and fungal symbioses. Science 303: 1361-1364.
Li RJ, Zhang CX, Fan SY, Wang YH, Wen J, Mysore KS, Xie ZP, Staehelin C. 2022. The Medicago truncatula hydrolase MtCHIT5b degrades Nod factors of Sinorhizobium meliloti and cooperates with MtNFH1 to regulate the nodule symbiosis. Frontiers in Plant Science 13: 1034230.
Li SC, Li YT. 1970. Studies on the glycosidases of jack bean meal. The Journal of Biological Chemistry 245: 5153-5160.
Liebminger E, Veit C, Pabst M, Batoux M, Zipfel C, Altmann F, Mach L, Strasser R. 2011. β-N-acetylhexosaminidases HEXO1 and HEXO3 are responsible for the formation of paucimannosidic N-glycans in Arabidopsis thaliana. The Journal of Biological Chemistry 286: 10793-10802.
Liu CW, Breakspear A, Guan D, Cerri MR, Jackson K, Jiang S, Robson F, Radhakrishnan GV, Roy S, Bone C et al. 2019. NIN acts as a network hub controlling a growth module required for rhizobial infection. Plant Physiology 179: 1704-1722.
Liu T, Duan Y, Yang Q. 2018. Revisiting glycoside hydrolase family 20 β-N-acetyl-d-hexosaminidases: crystal structures, physiological substrates and specific inhibitors. Biotechnology Advances 36: 1127-1138.
Liu Y, Yu SX, Xie ZP, Staehelin C. 2012. Analysis of a negative plant-soil feedback in a subtropical monsoon forest. Journal of Ecology 100: 1019-1028.
Luginbuehl LH, Menard GN, Kurup S, Van Erp H, Radhakrishnan GV, Breakspear A, Oldroyd GED, Eastmond PJ. 2017. Fatty acids in arbuscular mycorrhizal fungi are synthesized by the host plant. Science 356: 1175-1178.
Maillet F, Poinsot V, André O, Puech-Pagès V, Haouy A, Gueunier M, Cromer L, Giraudet D, Formey D, Niebel A et al. 2011. Fungal lipochitooligosaccharide symbiotic signals in arbuscular mycorrhiza. Nature 469: 58-63.
Malolepszy A, Kelly S, Sorensen KK, James EK, Kalisch C, Bozsoki Z, Panting M, Andersen SU, Sato S, Tao K et al. 2018. A plant chitinase controls cortical infection thread progression and nitrogen-fixing symbiosis. eLife 7: e38874.
Mitra RM, Gleason CA, Edwards A, Hadfield J, Downie JA, Oldroyd GE, Long SR. 2004. A Ca2+/calmodulin-dependent protein kinase required for symbiotic nodule development: gene identification by transcript-based cloning. Proceedings of the National Academy of Sciences, USA 101: 4701-4705.
Nadal M, Sawers R, Naseem S, Bassin B, Kulicke C, Sharman A, An G, An K, Ahern KR, Romag A et al. 2017. An N-acetylglucosamine transporter required for arbuscular mycorrhizal symbioses in rice and maize. Nature Plants 3: 17073.
Ovtsyna AO, Schultze M, Tikhonovich IA, Spaink HP, Kondorosi E, Kondorosi A, Staehelin C. 2000. Nod factors of Rhizobium leguminosarum bv. viciae and their fucosylated derivatives stimulate a Nod factor cleaving activity in pea roots and are hydrolyzed in vitro by plant chitinases at different rates. Molecular Plant-Microbe Interactions 13: 799-807.
Paszkowski U, Jakovleva L, Boller T. 2006. Maize mutants affected at distinct stages of the arbuscular mycorrhizal symbiosis. The Plant Journal 47: 165-173.
Perret X, Staehelin C, Broughton WJ. 2000. Molecular basis of symbiotic promiscuity. Microbiology and Molecular Biology Reviews 64: 180-201.
Pislariu CI, Murray JD, Wen J, Cosson V, Muni RR, Wang M, Benedito VA, Andriankaja A, Cheng X, Jerez IT et al. 2012. A Medicago truncatula tobacco retrotransposon insertion mutant collection with defects in nodule development and symbiotic nitrogen fixation. Plant Physiology 159: 1686-1699.
Price NP, Relić B, Talmont F, Lewin A, Promé D, Pueppke SG, Maillet F, Dénarié J, Promé JC, Broughton WJ. 1992. Broad-host-range Rhizobium species strain NGR234 secretes a family of carbamoylated, and fucosylated, nodulation signals that are O-acetylated or sulphated. Molecular Microbiology 6: 3575-3584.
Pueppke SG, Broughton WJ. 1999. Rhizobium sp. NGR234 and R. fredii USDA257 share exceptionally broad, nested host ranges. Molecular Plant-Microbe Interactions 12: 293-318.
Radutoiu S, Madsen LH, Madsen EB, Jurkiewicz A, Fukai E, Quistgaard EM, Albrektsen AS, James EK, Thirup S, Stougaard J. 2007. LysM domains mediate lipochitin-oligosaccharide recognition and Nfr genes extend the symbiotic host range. EMBO Journal 26: 3923-3935.
Rasmussen SR, Füchtbauer W, Novero M, Volpe V, Malkov N, Genre A, Bonfante P, Stougaard J, Radutoiu S. 2016. Intraradical colonization by arbuscular mycorrhizal fungi triggers induction of a lipochitooligosaccharide receptor. Scientific Reports 6: 29733.
Reissig JL, Strominger JL, Leloir LF. 1955. A modified colorimetric method for the estimation of N-acetylamino sugars. The Journal of Biological Chemistry 217: 959-966.
Roy S, Liu W, Nandety RS, Crook A, Mysore KS, Pislariu CI, Frugoli J, Dickstein R, Udvardi MK. 2020. Celebrating 20 years of genetic discoveries in legume nodulation and symbiotic nitrogen fixation. Plant Cell 32: 15-41.
Rush TA, Puech-Pages V, Bascaules A, Jargeat P, Maillet F, Haouy A, Maes AQ, Carriel CC, Khokhani D, Keller-Pearson M et al. 2020. Lipo-chitooligosaccharides as regulatory signals of fungal growth and development. Nature Communications 11: 3897.
Sagan M, deLarambergue H, Morandi D. 1998. Genetic analysis of symbiosis mutants in Medicago truncatula. In: Elmerich C, Kondorosi A, Newton WE, eds. Biological nitrogen fixation for the 21st century. Dordrecht, the Netherlands: Kluwer Academic, 317-318.
Schiessl K, Lilley JLS, Lee T, Tamvakis I, Kohlen W, Bailey PC, Thomas A, Luptak J, Ramakrishnan K, Carpenter MD et al. 2019. NODULE INCEPTION recruits the lateral root developmental program for symbiotic nodule organogenesis in Medicago truncatula. Current Biology 29: 3657-3668.
Schultze M, Quiclet-Sire B, Kondorosi E, Virelizer H, Glushka JN, Endre G, Géro SD, Kondorosi A. 1992. Rhizobium meliloti produces a family of sulfated lipooligosaccharides exhibiting different degrees of plant host specificity. Proceedings of the National Academy of Sciences, USA 89: 192-196.
Schultze M, Staehelin C, Brunner F, Genetet I, Legrand M, Fritig B, Kondorosi E, Kondorosi A. 1998. Plant chitinase/lysozyme isoforms show distinct substrate specificity and cleavage site preference towards lipochitooligosaccharide Nod signals. The Plant Journal 16: 571-580.
Smith SE, Read D. 2008. Mycorrhizal symbiosis. Cambridge, UK: Academic Press.
Spaink HP, Sheeley DM, van Brussel AA, Glushka J, York WS, Tak T, Geiger O, Kennedy EP, Reinhold VN, Lugtenberg BJ. 1991. A novel highly unsaturated fatty acid moiety of lipo-oligosaccharide signals determines host specificity of Rhizobium. Nature 354: 125-130.
Staehelin C, Granado J, Müller J, Wiemken A, Mellor RB, Felix G, Regenass M, Broughton WJ, Boller T. 1994a. Perception of Rhizobium nodulation factors by tomato cells and inactivation by root chitinases. Proceedings of the National Academy of Sciences, USA 91: 2196-2200.
Staehelin C, Schultze M, Kondorosi E, Mellor RB, Boller T, Kondorosi A. 1994b. Structural modifications in Rhizobium meliloti Nod factors influence their stability against hydrolysis by root chitinases. The Plant Journal 5: 319-330.
Staehelin C, Xie ZP, Illana A, Vierheilig H. 2011. Long-distance transport of signals during symbiosis: are nodule formation and mycorrhization autoregulated in a similar way? Plant Signaling & Behavior 6: 372-377.
Strasser R, Bondili JS, Schoberer J, Svoboda B, Liebminger E, Glössl J, Altmann F, Steinkellner H, Mach L. 2007. Enzymatic properties and subcellular localization of Arabidopsis β-N-acetylhexosaminidases. Plant Physiology 145: 5-16.
Sun J, Miller JB, Granqvist E, Wiley-Kalil A, Gobbato E, Maillet F, Cottaz S, Samain E, Venkateshwaran M, Fort S et al. 2015. Activation of symbiosis signaling by arbuscular mycorrhizal fungi in legumes and rice. Plant Cell 27: 823-838.
Tadege M, Wen J, He J, Tu H, Kwak Y, Eschstruth A, Cayrel A, Endre G, Zhao PX, Chabaud M et al. 2008. Large-scale insertional mutagenesis using the Tnt1 retrotransposon in the model legume Medicago truncatula. The Plant Journal 54: 335-347.
Tian Y, Liu W, Cai J, Zhang LY, Wong KB, Feddermann N, Boller T, Xie ZP, Staehelin C. 2013. The nodulation factor hydrolase of Medicago truncatula: characterization of an enzyme specifically cleaving rhizobial nodulation signals. Plant Physiology 163: 1179-1190.
Tominaga T, Yao L, Saito H, Kaminaka H. 2022. Conserved and diverse transcriptional reprogramming triggered by the establishment of symbioses in tomato roots forming Arum-type and Paris-type arbuscular mycorrhizae. Plants 11: 747.
Trinh TH, Ratet P, Kondorosi E, Durand P, Kamaté K, Bauer P, Kondorosi A. 1998. Rapid and efficient transformation of diploid Medicago truncatula and Medicago sativa ssp. falcata lines improved in somatic embryogenesis. Plant Cell Reports 17: 345-355.
Tsujimori Y, Ogura M, Rahman MZ, Maeda M, Kimura Y. 2019. Plant complex type free N-glycans occur in tomato xylem sap. Bioscience Biotechnology Biochemistry 83: 1310-1314.
Van Brussel AAN, Tak T, Wetselaar A, Pees E, Wijffelman C. 1982. Small leguminosae as test plants for nodulation of Rhizobium leguminosarum and other rhizobia and agrobacteria harbouring a leguminosarum sym-plasmid. Plant Science Letters 27: 317-325.
Vierheilig H, Coughlan AP, Wyss U, Piche Y. 1998. Ink and vinegar, a simple staining technique for arbuscular-mycorrhizal fungi. Applied and Environmental Microbiology 64: 5004-5007.
Volpe V, Chialva M, Mazzarella T, Crosino A, Capitanio S, Costamagna L, Kohlen W, Genre A. 2023. Long-lasting impact of chitooligosaccharide application on strigolactone biosynthesis and fungal accommodation promotes arbuscular mycorrhiza in Medicago truncatula. New Phytologist 237: 2316-2331.
Walker L, Lagunas B, Gifford ML. 2020. Determinants of host range specificity in legume-rhizobia symbiosis. Frontiers in Microbiology 11: 585749.
Wang D, Dong W, Murray J, Wang E. 2022. Innovation and appropriation in mycorrhizal and rhizobial symbioses. Plant Cell 34: 1573-1599.
Yang J, Lan L, Jin Y, Yu N, Wang D, Wang E. 2022. Mechanisms underlying legume-rhizobium symbioses. Journal of Integrative Plant Biology 64: 244-267.
Zeng T, Holmer R, Hontelez J, Te Lintel-Hekkert B, Marufu L, de Zeeuw T, Wu F, Schijlen E, Bisseling T, Limpens E. 2018. Host- and stage-dependent secretome of the arbuscular mycorrhizal fungus Rhizophagus irregularis. The Plant Journal 94: 411-425.
Zeng T, Rodriguez-Moreno L, Mansurkhodzaev A, Wang P, van den Berg W, Gasciolli V, Cottaz S, Fort S, Thomma B, Bono JJ et al. 2020. A lysin motif effector subverts chitin-triggered immunity to facilitate arbuscular mycorrhizal symbiosis. New Phytologist 225: 448-460.
Zeng Z, Liu Y, Feng XY, Li SX, Jiang XM, Chen JQ, Shao ZQ. 2023. The RNAome landscape of tomato during arbuscular mycorrhizal symbiosis reveals an evolving RNA layer symbiotic regulatory network. Plant Communications 4: 100429.
Zhang C, He J, Dai H, Wang G, Zhang X, Wang C, Shi J, Chen X, Wang D, Wang E. 2021. Discriminating symbiosis and immunity signals by receptor competition in rice. Proceedings of the National Academy of Sciences, USA 118: e2023738118.