Abstract
Many reviews report induction of defence genes similar with pathogenesis in legume-rhizobia and mycorrhizal symbioses, suggesting it could be a convergent point in plant-microorganism symbiotic systems. However, research in actinorhizal symbiosis versus pathogenesis is still in early stages and much remains to be learned to confirm this hypothesis. Here, we review studies on plant immune system in actinorhizal symbiosis, focusing on Alnus glutinosa, one of the best studied actinorhizal plants, for which genomic and transcriptomic data have recently been published. This review draws up the first overview of plant immune reactions during the Frankia-Alnus symbiosis and summarises all evidence of (i) a putative transient expression of defence genes during the early steps of symbiosis establishment in Alnus-Frankia interactions, and (ii) defence genes highly expressed in mature and functional root nodules in which the microbial partner is hosted. These genes are related to three main host plant stress response categories: oxidative stress response, Pathogenesis-Related (PR) proteins and Systemic Acquired Resistance (SAR). Their putative key role in plant–microbe interactions is discussed, with the major challenge being to understand to what extent they would be related to symbiosis, to stress response, or both.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Ahmadizadeh M, Chen J-T, Hasanzadeh S, Ahmar S, Heidari P (2020) Insights into the genes involved in the ethylene biosynthesis pathway in Arabidopsis thaliana and Oryza sativa. J Genet Eng Biotechnol 18:62. https://doi.org/10.1186/s43141-020-00083-1
Akkermans A, Hahn D, Zoon F (1989) Interactions between root symbionts, root pathogens and actinorhizal plants. Ann Sci for 46:765s–771s. https://doi.org/10.1051/forest:198905ART0171
Alhoraibi H, Bigeard J, Rayapuram N, Colcombet J, Hirt H (2019) Plant Immunity: The MTI-ETI Model and Beyond. Current Issues in Molecular Biology 30: 39–58. https://doi.org/10.21775/cimb.030.039
Ali S, Ganai BA, Kamili AN, Bhat AA, Mir ZA, Bhat JA, Tyagi A, Islam ST, Mushtaq M, Yadav P et al (2018) Pathogenesis-related proteins and peptides as promising tools for engineering plants with multiple stress tolerance. Microbiol Res 212–213:29–37. https://doi.org/10.1016/j.micres.2018.04.008
Anderson JC, Wan Y, Kim Y-M, Pasa-Tolic L, Metz TO, Peck SC (2014) Decreased abundance of type III secretion system-inducing signals in Arabidopsis mkp1 enhances resistance against Pseudomonas syringae. Proc Natl Acad Sci 111:6846–6851. https://doi.org/10.1073/pnas.1403248111
Axtell MJ, Staskawicz BJ (2003) Initiation of RPS2-Specified Disease Resistance in Arabidopsis Is Coupled to the AvrRpt2-Directed Elimination of RIN4. Cell 112:369–377. https://doi.org/10.1016/S0092-8674(03)00036-9
Backer R, Naidoo S, van den Berg N (2019) The nonexpressor of pathogenesis-related genes 1 (NPR1) and related family: mechanistic insights in plant disease resistance. Front Plant Sci 10:102. https://doi.org/10.3389/fpls.2019.00102
Balint-Kurti P (2019) The plant hypersensitive response: concepts, control and consequences. Mol Plant Pathol 20:1163–1178. https://doi.org/10.1111/mpp.12821
Bari R, Jones JDG (2009) Role of plant hormones in plant defence responses. Plant Mol Biol 69:473–488. https://doi.org/10.1007/s11103-008-9435-0
Baxter A, Mittler R, Suzuki N (2014) ROS as key players in plant stress signalling. J Exp Bot 65:1229–1240. https://doi.org/10.1093/jxb/ert375
Becana M, Matamoros MA, Udvardi M, Dalton DA (2010) Recent insights into antioxidant defenses of legume root nodules. New Phytol 188:960–976. https://doi.org/10.1111/j.1469-8137.2010.03512.x
Berry AM, McIntyre L, McCully ME (1986) Fine structure of root hair infection leading to nodulation in the Frankia-Alnus symbiosis. Can J Bot 64:292–305. https://doi.org/10.1139/b86-043
Bigeard J, Colcombet J, Hirt H (2015) Signaling Mechanisms in Pattern-Triggered Immunity (PTI). Mol Plant 8:521–539. https://doi.org/10.1016/j.molp.2014.12.022
Bonfante P, Genre A (2010) Mechanisms underlying beneficial plant–fungus interactions in mycorrhizal symbiosis. Nat Commun 1:48. https://doi.org/10.1038/ncomms1046
Brasier CM, Rose J, Gibbs JN (1995) An unusual Phytophthora associated with widespread alder mortality in Britain. Plant Pathol 44:999–1007. https://doi.org/10.1111/j.1365-3059.1995.tb02658.x
Brasier C, Kirk S, Delcan C, Jung T, Veld M (2004) Phytophthora alni sp. nov. and its variants: Designation of emerging heteroploid hybrid pathogens spreading on Alnus trees. Mycol Res 108:1172–1184. https://doi.org/10.1017/S0953756204001005
Brechenmacher L, Kim M-Y, Benitez M, Li M, Joshi T, Calla B, Lee MP, Libault M, Vodkin LO, Xu D et al (2008) Transcription Profiling of Soybean Nodulation by Bradyrhizobium japonicum. MPMI 21:631–645. https://doi.org/10.1094/MPMI-21-5-0631
Breen S, Williams SJ, Outram M, Kobe B, Solomon PS (2017) Emerging Insights into the Functions of Pathogenesis-Related Protein 1. Trends Plant Sci 22:871–879. https://doi.org/10.1016/j.tplants.2017.06.013
Breitenbach HH, Wenig M, Wittek F, Jordá L, Maldonado-Alconada AM, Sarioglu H, Colby T, Knappe C, Bichlmeier M, Pabst E et al (2014) Contrasting Roles of the Apoplastic Aspartyl Protease APOPLASTIC, ENHANCED DISEASE SUSCEPTIBILITY1-DEPENDENT1 and LEGUME LECTIN-LIKE PROTEIN1 in Arabidopsis Systemic Acquired Resistance. Plant Physiol 165:791–809. https://doi.org/10.1104/pp.114.239665
Cano LM, Raffaele S, Haugen RH, Saunders DGO, Leonelli L, MacLean D, Hogenhout SA, Kamoun S (2013) Major Transcriptome Reprogramming Underlies Floral Mimicry Induced by the Rust Fungus Puccinia monoica in Boechera stricta. PLoS One 8:e75293. https://doi.org/10.1371/journal.pone.0075293
Carrere S, Verdier J, Gamas P (2021) MtExpress, a Comprehensive and Curated RNAseq-based Gene Expression Atlas for the Model Legume Medicago truncatula. Plant Cell Physiol 62:1494–1500. https://doi.org/10.1093/pcp/pcab110
Carro L, Pujic P, Alloisio N, Fournier P, Boubakri H, Hay AE, Poly F, François P, Hocher V, Mergaert P et al (2015) Alnus peptides modify membrane porosity and induce the release of nitrogen-rich metabolites from nitrogen-fixing Frankia. ISME J 9:1723–1733. https://doi.org/10.1038/ismej.2014.257
Carro L, Pujic P, Alloisio N, Fournier P, Boubakri H, Poly F, Rey M, Heddi A, Normand P (2016) Physiological effects of major up-regulated Alnus glutinosa peptides on Frankia sp. ACN14a. Microbiology 162: 1173–1184. https://doi.org/10.1099/mic.0.000291
Chen HY, Hsieh EJ, Cheng MC, Chen CY, Hwang SY, Lin TP (2016) ORA47 (octadecanoid-responsive AP2/ERF-domain transcription factor 47) regulates jasmonic acid and abscisic acid biosynthesis and signaling through binding to a novel cis-element. New Phytol 211:599–613. https://doi.org/10.1111/nph.13914
Chen X, Shang J, Chen D, Lei C, Zou Y, Zhai W, Liu G, Xu J, Ling Z, Cao G et al (2006) A B-lectin receptor kinase gene conferring rice blast resistance. Plant J 46:794–804. https://doi.org/10.1111/j.1365-313X.2006.02739.x
Choi MS, Kim W, Lee C, Oh CS (2013) Harpins, Multifunctional Proteins Secreted by Gram-Negative Plant-Pathogenic Bacteria. MPMI 26:1115–1122. https://doi.org/10.1094/MPMI-02-13-0050-CR
Coll NS, Epple P, Dangl JL (2011) Programmed cell death in the plant immune system. Cell Death Differ 18:1247–1256. https://doi.org/10.1038/cdd.2011.37
Collum TD, Culver JN (2016) The impact of phytohormones on virus infection and disease. Curr Opin Virol 17:25–31. https://doi.org/10.1016/j.coviro.2015.11.003
Conesa A, Götz S (2008) Blast2GO: A Comprehensive Suite for Functional Analysis in Plant Genomics. Int J Plant Genomics 2008:1–12. https://doi.org/10.1155/2008/619832
Dellagi A, Rigault M, Segond D, Roux C, Kraepiel Y, Cellier F, Briat JF, Gaymard F, Expert D (2005) Siderophore-mediated upregulation of Arabidopsis ferritin expression in response to Erwinia chrysanthemi infection. Plant J 43:262–272. https://doi.org/10.1111/j.1365-313X.2005.02451.x
Demina IV, Persson T, Santos P, Plaszczyca M, Pawlowski K (2013) Comparison of the nodule vs. root transcriptome of the actinorhizal plant datisca glomerata: actinorhizal nodules contain a specific class of defensins. PLOS One 8:e72442. https://doi.org/10.1371/journal.pone.0072442
Dixon MS, Jones DA, Keddie JS, Thomas CM, Harrison K, Jones JDG (1996) The tomato Cf-2 disease resistance locus comprises two functional genes encoding leucine-rich repeat proteins. Cell 84:451–459. https://doi.org/10.1016/S0092-8674(00)81290-8
Dixon RA, Achnine L, Kota P, Liu CJ, Reddy MSS, Wang L (2002) The phenylpropanoid pathway and plant defence—a genomics perspective. Mol Plant Pathol 3:371–390. https://doi.org/10.1046/j.1364-3703.2002.00131.x
Dodds PN, Rathjen JP (2010) Plant immunity: towards an integrated view of plant–pathogen interactions. Nat Rev Genet 11:539–548. https://doi.org/10.1038/nrg2812
Dow M, Newman MA, von Roepenack E (2000) The Induction and Modulation of Plant Defense Responses by Bacterial Lipopolysaccharides. Annu Rev Phytopathol 38:241–261. https://doi.org/10.1146/annurev.phyto.38.1.241
Durrant WE, Dong X (2004) Systemic acquired resistance. Annu Rev Phytopathol 42:185–209. https://doi.org/10.1146/annurev.phyto.42.040803.140421
Faulkner C, Petutschnig E, Benitez-Alfonso Y, Beck M, Robatzek S, Lipka V, Maule AJ (2013) LYM2-dependent chitin perception limits molecular flux via plasmodesmata. Proc Natl Acad Sci 110:9166–9170. https://doi.org/10.1073/pnas.1203458110
Fawke S, Doumane M, Schornack S (2015) Oomycete Interactions with Plants: Infection Strategies and Resistance Principles. Microbiol Mol Biol Rev 79:263–280 https://doi.org/10.1128/MMBR.00010-15
Feys BJ, Parker JE (2000) Interplay of signaling pathways in plant disease resistance. Trends Genet 16:449–455. https://doi.org/10.1016/S0168-9525(00)02107-7
Fortunato A, Santos P, Graça I, Gouveia MM, Martins SM, Pinto Ricardo CP, Pawlowski K, Ribeiro A (2007) Isolation and characterization of cgchi3, a nodule-specific gene from Casuarina glauca encoding a class III chitinase. Physiol Plant 130:418–426. https://doi.org/10.1111/j.1399-3054.2006.00864.x
Fu ZQ, Dong X (2013) Systemic acquired resistance: turning local infection into global defense. Annu Rev Plant Biol 64:839–863. https://doi.org/10.1146/annurev-arplant-042811-105606
Fujita K, Inui H (2021) Review: Biological functions of major latex-like proteins in plants. Plant Sci 306:110856. https://doi.org/10.1016/j.plantsci.2021.110856
Gallie DR (2015) Ethylene receptors in plants - why so much complexity? F1000Prime Rep 7. https://doi.org/10.12703/P7-39
García-Garrido JM, Ocampo JA (2002) Regulation of the plant defence response in arbuscular mycorrhizal symbiosis. J Exp Bot 53:1377–1386. https://doi.org/10.1093/jexbot/53.373.1377
Gasser M, Alloisio N, Fournier P, Balmand S, Kharrat O, Tulumello J, Carro L, Heddi A, Da Silva P, Normand P et al (2022) A non specific Lipid Transfer Protein with potential functions in infection and nodulation. MPMI. https://doi.org/10.1094/MPMI-06-22-0131-R
Genre A, Russo G (2016) Does a common pathway transduce symbiotic signals in plant-microbe interactions? Front Plant Sci 7:96. https://doi.org/10.3389/fpls.2016.00096
Glazebrook J (2001) Genes controlling expression of defense responses in Arabidopsis — 2001 status. Curr Opin Plant Biol 4:301–308. https://doi.org/10.1016/S1369-5266(00)00177-1
Goetting-Minesky MP, Mullin BC (1994) Differential gene expression in an actinorhizal symbiosis: evidence for a nodule-specific cysteine proteinase. Proc Natl Acad Sci 91:9891–9895. https://doi.org/10.1104/pp.111.174151
Golshani F, Fakheri B, Behshad E, Vashvaei RM (2015) PRs proteins and their Mechanism in Plants. In: Biological Forum: Research Trend 7:477–495
Gourion B, Berrabah F, Ratet P, Stacey G (2015) Rhizobium–legume symbioses: the crucial role of plant immunity. Trends Plant Sci 20:186–194. https://doi.org/10.1016/j.tplants.2014.11.008
Granqvist E, Sun J, Op den Camp R, Pujic P, Hill L, Normand P, Morris RJ, Downie JA, Geurts R, Oldroyd GED (2015) Bacterial-induced calcium oscillations are common to nitrogen-fixing associations of nodulating legumes and non-legumes. New Phytol 207:551–558. https://doi.org/10.1111/nph.13464
Grant M, Lamb C (2006) Systemic immunity. Curr Opin Plant Biol 9:414–420. https://doi.org/10.1016/j.pbi.2006.05.013
Griesmann M, Chang Y, Liu X, Song Y, Haberer G, Crook MB, Billault-Penneteau B, Lauressergues D, Keller J, Imanishi L, et al (2018) Phylogenomics reveals multiple losses of nitrogen-fixing root nodule symbiosis. Science 361:eaat1743. https://doi.org/10.1126/science.aat1743
Gucciardo S, Wisniewski J-P, Brewin NJ, Bornemann S (2007) A germin-like protein with superoxide dismutase activity in pea nodules with high protein sequence identity to a putative rhicadhesin receptor. J Exp Bot 58:1161–1171. https://doi.org/10.1093/jxb/erl282
Hammad Y, Nalin R, Marechal J, Fiasson K, Pepin R, Berry AM, Normand P, Domenach A-M (2003) A possible role for phenyl acetic acid (PAA) on Alnus glutinosa nodulation by Frankia. In: Normand P, Dawson JO, Pawlowski K, eds. Frankia Symbiosis. Springer Netherlands, Dordrecht, 193–205
Hao Z, Xie W, Chen B (2019) Arbuscular Mycorrhizal Symbiosis Affects Plant Immunity to Viral Infection and Accumulation. Viruses 11:534. https://doi.org/10.3390/v11060534
He S, Yuan G, Bian S, Han X, Liu K, Cong P, Zhang C (2020) Major Latex Protein MdMLP423 Negatively Regulates Defense against Fungal Infections in Apple. Int J Mol Sci 21:1879. https://doi.org/10.3390/ijms21051879
Herlihy J, Ludwig NR, van den Ackerveken G, McDowell JM (2019) Oomycetes Used in Arabidopsis Research. Arabidopsis Book 17:e0188. https://doi.org/10.1199/tab.0188
Hocher V, Alloisio N, Auguy F, Fournier P, Doumas P, Pujic P, Gherbi H, Queiroux C, Da Silva C, Wincker P et al (2011) Transcriptomics of Actinorhizal Symbioses Reveals Homologs of the Whole Common Symbiotic Signaling Cascade. Plant Physiol 156:700–711. https://doi.org/10.1104/pp.111.174151
Hocher V, Ngom M, Carré-Mlouka A, Tisseyre P, Gherbi H, Svistoonoff S (2019) Signalling in actinorhizal root nodule symbioses. Antonie Van Leeuwenhoek 112:23–29. https://doi.org/10.1007/s10482-018-1182-x
Hogenhout SA, Van der Hoorn RAL, Terauchi R, Kamoun S (2009) Emerging Concepts in Effector Biology of Plant-Associated Organisms. MPMI 22:115–122. https://doi.org/10.1094/MPMI-22-2-0115
Hua J, Sakai H, Nourizadeh S, Chen QG, Bleecker AB, Ecker JR, Meyerowitz EM (1998) EIN4 and ERS2 Are Members of the Putative Ethylene Receptor Gene Family in Arabidopsis. Plant Cell 10:1321–1332. https://doi.org/10.1105/tpc.10.8.1321
Huang S, Vossen EAGVD, Kuang H, Vleeshouwers VGAA, Zhang N, Borm TJA, Eck HJV, Baker B, Jacobsen E, Visser RGF (2005) Comparative genomics enabled the isolation of the R3a late blight resistance gene in potato. Plant J 42:251–261. https://doi.org/10.1111/j.1365-313X.2005.02365.x
Hwang IS, Choi DS, Kim NH, Kim DS, Hwang BK (2014) Pathogenesis-related protein 4b interacts with leucine-rich repeat protein 1 to suppress PR4b-triggered cell death and defense response in pepper. Plant Journal 77:521–533. https://doi.org/10.1111/tpj.12400
Iven T, König S, Singh S, Braus-Stromeyer SA, Bischoff M, Tietze LF, Braus GH, Lipka V, Feussner I, Dröge-Laser W (2012) Transcriptional activation and production of tryptophan-derived secondary metabolites in arabidopsis roots contributes to the defense against the fungal vascular pathogen verticillium longisporum. Mol Plant 5:1389–1402. https://doi.org/10.1093/mp/sss044
Johnson LJ, Johnson RD, Schardl CL, Panaccione DG (2003) Identification of differentially expressed genes in the mutualistic association of tall fescue with Neotyphodium coenophialum. Physiol Mol Plant Pathol 63:305–317. https://doi.org/10.1016/j.pmpp.2004.04.001
Jones JDG, Dangl JL (2006) The plant immune system. Nature 444:323–329. https://doi.org/10.1038/nature05286
Jung HW, Tschaplinski TJ, Wang L et al (2009) Priming in Systemic Plant Immunity. Science 324:89–91. https://doi.org/10.1126/science.1170025
Karmakar K, Kundu A, Rizvi AZ, Dubois E, Severac D, Czernic P, Cartieaux F, DasGupta M (2019) Transcriptomic analysis with the progress of symbiosis in ‘Crack-Entry’ legume arachis hypogaea highlights its contrast with ‘Infection Thread’ Adapted Legumes. Molecular Plant-Microbe Interactions 32:271–285. https://doi.org/10.1094/MPMI-06-18-0174-R
Kawaharada Y, Kelly S, Nielsen MW, Hjuler CT, Gysel K, Muszyński A, Carlson RW, Thygesen MB, Sandal N, Asmussen MH et al (2015) Receptor-mediated exopolysaccharide perception controls bacterial infection. Nature 523:308–312. https://doi.org/10.1038/nature14611
Kistner C, Parniske M (2002) Evolution of signal transduction in intracellular symbiosis. Trends Plant Sci 7:511–518. https://doi.org/10.1016/S1360-1385(02)02356-7
Kunkel BN, Brooks DM (2002) Cross talk between signaling pathways in pathogen defense. Curr Opin Plant Biol 5:325–331. https://doi.org/10.1016/S1369-5266(02)00275-3
Kuźniak E, Urbanek H (2000) The involvement of hydrogen peroxide in plant responses to stresses. Acta Physiol Plant 22:195–203. https://doi.org/10.1007/s11738-000-0076-4
Laplaze L, Ribeiro A, Franche C, Duhoux E, Auguy F, Bogusz D, Pawlowski K (2000) Characterization of a Casuarina glauca Nodule-Specific Subtilisin-like Protease Gene, a Homolog of Alnus glutinosa ag12. MPMI 13:113–117. https://doi.org/10.1094/MPMI.2000.13.1.113
Lay FT, Anderson MA (2005) Defensins - Components of the Innate Immune System in Plants. Curr Protein Pept Sci 6:85–101. https://doi.org/10.2174/1389203053027575
Liu B, Li J-F, Ao Y, Qu J, Li Z, Su J, Zhang Y, Liu J, Feng D, Qi K et al (2012) Lysin motif–containing proteins LYP4 and LYP6 play dual roles in peptidoglycan and chitin perception in rice innate immunity. Plant Cell 24:3406–3419. https://doi.org/10.1105/tpc.112.102475
Liu F, Zhang X, Lu C, Zeng X, Li Y, Fu D, Wu G (2015) Non-specific lipid transfer proteins in plants: presenting new advances and an integrated functional analysis. J Exp Bot 66:5663–5681. https://doi.org/10.1093/jxb/erv313
Liu G, Liu J, Zhang C, You X, Zhao T, Jiang J, Chen X, Zhang H, Yang H, Zhang D et al (2018) Physiological and RNA-seq analyses provide insights into the response mechanism of the Cf-10-mediated resistance to Cladosporium fulvum infection in tomato. Plant Mol Biol 96:403–416. https://doi.org/10.1007/s11103-018-0706-0
Liu S, Wu J, Zhang P, Hasi G, Huang Y, Lu J, Zhang Y (2016) Response of phytohormones and correlation of SAR signal pathway genes to the different resistance levels of grapevine against Plasmopara viticola infection. Plant Physiol Biochem 107:56–66. https://doi.org/10.1016/j.plaphy.2016.05.020
Mackey D, Belkhadir Y, Alonso JM, Ecker JR, Dangl JL (2003) Arabidopsis RIN4 Is a Target of the Type III Virulence Effector AvrRpt2 and Modulates RPS2-Mediated Resistance. Cell 112:379–389. https://doi.org/10.1016/S0092-8674(03)00040-0
Mauch-Mani B, Mauch F (2005) The role of abscisic acid in plant–pathogen interactions. Curr Opin Plant Biol 8:409–414. https://doi.org/10.1016/j.pbi.2005.05.015
Missaoui K, Gonzalez-Klein Z, Pazos-Castro D, Hernandez-Ramirez G, Garrido-Arandia M, Brini F, Diaz-Perales A, Tome-Amat J (2022) Plant non-specific lipid transfer proteins: An overview. Plant Physiol Biochem 171:115–127. https://doi.org/10.1016/j.plaphy.2021.12.026
Molina A, Segura A, García-Olmedo F (1993) Lipid transfer proteins (nsLTPs) from barley and maize leaves are potent inhibitors of bacterial and fungal plant pathogens. FEBS Lett 316:119–122. https://doi.org/10.1016/0014-5793(93)81198-9
Mosher S, Kemmerling B (2013) PSKR1 and PSY1R-mediated regulation of plant defense responses. Plant Signal Behav 8:e24119. https://doi.org/10.4161/psb.24119
Nanda AK, Andrio E, Marino D, Pauly N, Dunand C (2010) Reactive Oxygen Species during Plant-microorganism Early Interactions. J Integr Plant Biol 52:195–204. https://doi.org/10.1111/j.1744-7909.2010.00933.x
Nave C, Schwan J, Werres S, Riebesehl J (2021) Alnus glutinosa Threatened by Alder Phytophthora: A Histological Study of Roots. Pathogens 10:977. https://doi.org/10.3390/pathogens10080977
Newman MA, Von Roepenack-Lahaye E, Parr A, Daniels MJ, Dow JM (2002) Prior exposure to lipopolysaccharide potentiates expression of plant defenses in response to bacteria. Plant J 29:487–495. https://doi.org/10.1046/j.0960-7412.2001.00233.x
Nürnberger T, Lipka V (2005) Non-host resistance in plants: new insights into an old phenomenon. Mol Plant Pathol 6:335–345. https://doi.org/10.1111/j.1364-3703.2005.00279.x
Park E-J, Kim T-H (2021) Arabidopsis OSMOTIN 34 Functions in the ABA Signaling Pathway and Is Regulated by Proteolysis. Int J Mol Sci 22:7915. https://doi.org/10.3390/ijms22157915
Pawlowski K, Swensen S, Guan C, Hadri A-E, Berry AM, Bisseling T (2003) Distinct Patterns of Symbiosis-Related Gene Expression in Actinorhizal Nodules from Different Plant Families. Mol Plant-Microbe Interact® 16:796–807. https://doi.org/10.1071/FP11066
Pawlowski K, Bogusz D, Ribeiro A, Berry AM, Pawlowski K, Bogusz D, Ribeiro A, Berry AM (2011) Progress on research on actinorhizal plants. Funct Plant Biol 38:633–638. https://doi.org/10.1071/FP11066
Pawlowski K, Demchenko KN (2012) The diversity of actinorhizal symbiosis. Protoplasma 249:967–979. https://doi.org/10.1007/s00709-012-0388-4
Pawlowski K, Sprent JI (2008) Comparison Between Actinorhizal And Legume Symbiosis. In: Pawlowski K, Newton WE (eds) Nitrogen-fixing Actinorhizal Symbioses. Springer, Netherlands, Dordrecht, pp 261–288
Peleg-Grossman S, Volpin H, Levine A (2007) Root hair curling and Rhizobium infection in Medicago truncatula are mediated by phosphatidylinositide-regulated endocytosis and reactive oxygen species. J Exp Bot 58:1637–1649. https://doi.org/10.1093/jxb/erm013
Peleg-Grossman S, Melamed-Book N, Levine A (2012) ROS production during symbiotic infection suppresses pathogenesis-related gene expression. Plant Signal Behav 7:409–415. https://doi.org/10.4161/psb.19217
Peng JL, Dong HS, Dong HP, Delaney TP, Bonasera JM, Beer SV (2003) Harpin-elicited hypersensitive cell death and pathogen resistance require the NDR1 and EDS1 genes. Physiol Mol Plant Pathol 62:317–326. https://doi.org/10.1016/S0885-5765(03)00078-X
Porter SS, Bantay R, Friel CA, Garoutte A, Gdanetz K, Ibarreta K, Moore BM, Shetty P, Siler E, Friesen ML (2020) Beneficial microbes ameliorate abiotic and biotic sources of stress on plants. Funct Ecol 34:2075–2086. https://doi.org/10.1111/1365-2435.13499
Pozo MJ, Azcón-Aguilar C (2007) Unraveling mycorrhiza-induced resistance. Curr Opin Plant Biol 10:393–398. https://doi.org/10.1016/j.pbi.2007.05.004
Pozzi AC, Bautista-Guerrero HH, Nouioui I, Cotin-Galvan L, Pepin R, Fournier P, Menu F, Fernandez MP, Herrera-Belaroussi A (2015) In-planta sporulation phenotype: a major life history trait to understand the evolution of Alnus-infective Frankia strains. Environ Microbiol 17:3125–3138. https://doi.org/10.1111/1462-2920.12644
Prasannath K (2017) Plant defense-related enzymes against pathogens: a review. AGRIEAST: J Agric Sci 11:38 https://doi.org/10.4038/agrieast.v11i1.33
Redondo MA, Boberg J, Olsson CHB, Oliva J (2015) Winter Conditions Correlate with Phytophthora alni Subspecies Distribution in Southern Sweden. Phytopathology® 105:1191–1197. https://doi.org/10.1094/PHYTO-01-15-0020-R
Ribeiro A, Akkermans AD, van Kammen A, Bisseling T, Pawlowski K (1995) A nodule-specific gene encoding a subtilisin-like protease is expressed in early stages of actinorhizal nodule development. Plant Cell 7:785–794. https://doi.org/10.1105/tpc.7.6.785
Ribeiro A, Graça I, Pawlowski K, Santos P, Ribeiro A, Graça I, Pawlowski K, Santos P (2011) Actinorhizal plant defence-related genes in response to symbiotic Frankia. Funct Plant Biol 38:639–644. https://doi.org/10.1071/FP11012
Roman ML, Izarra M, Lindqvist-Kreuze H, Rivera C, Gamboa S, Tovar JC, Forbes GA, Kreuze JF, Ghislain M (2017) R/Avr gene expression study of Rpi-vnt1.1 transgenic potato resistant to the Phytophthora infestans clonal lineage EC-1. Plant Cell Tissue Organ Cult 131:259–268. https://doi.org/10.1007/s11240-017-1281-9
Ron M, Avni A (2004) The receptor for the fungal elicitor ethylene-inducing xylanase is a member of a resistance-like gene family in tomato. Plant Cell 16:1604–1615. https://doi.org/10.1105/tpc.022475
Ruan J, Zhou Y, Zhou M, Yan J, Khurshid M, Weng W, Cheng J, Zhang K (2019) Jasmonic Acid Signaling Pathway in Plants. Int J Mol Sci 20:2479. https://doi.org/10.3390/ijms20102479
Salgado MG, Demina IV, Maity PJ, Nagchowdhury A, Caputo A, Krol E, Loderer C, Muth G, Becker A, Pawlowski K (2022) Legume NCRs and nodule-specific defensins of actinorhizal plants—Do they share a common origin? PLOS One 17:e0268683. https://doi.org/10.1371/journal.pone.0268683
Salzer P, Bonanomi A, Beyer K, Vögeli-Lange R, Aeschbacher RA, Lange J, Wiemken A, Kim D, Cook DR, Boller T (2000) Differential Expression of Eight Chitinase Genes in Medicago truncatula Roots During Mycorrhiza Formation, Nodulation, and Pathogen Infection. MPMI 13:763–777. https://doi.org/10.1094/MPMI.2000.13.7.763
Santos P, Fortunato A, Graça I, Martins SM, Gouveia MM, Auguy F, Bogusz D, Ricardo CPP, Pawlowski K, Ribeiro A (2010) Characterization of four defense-related genes up-regulated in root nodules of Casuarina glauca. Symbiosis 50:27–35. https://doi.org/10.1007/s13199-009-0031-0
Schenk PM, Kazan K, Rusu AG, Manners JM, Maclean DJ (2005) The SEN1 gene of Arabidopsis is regulated by signals that link plant defence responses and senescence. Plant Physiol Biochem 43:997–1005. https://doi.org/10.1016/j.plaphy.2005.09.002
Segura A, Moreno M, Molina A, Garcı́a-Olmedo F (1998) Novel defensin subfamily from spinach (Spinacia oleracea). FEBS Lett 435:159–162. https://doi.org/10.1016/S0014-5793(98)01060-6
Sikorski MM, Biesiadka J, Kasperska AE, Kopcińska J, Łotocka B, Golinowski W, Legocki AB (1999) Expression of genes encoding PR10 class pathogenesis-related proteins is inhibited in yellow lupine root nodules. Plant Sci 149:125–137. https://doi.org/10.1016/S0168-9452(99)00148-X
Song R, Li J, Xie C, Jian W, Yang X (2020a) Identification and functional characterization of NbMLP28, a novel MLP-like protein 28 enhancing Potato virus Y resistance in Nicotiana benthamiana. BMC Microbiol 20:1–14. https://doi.org/10.1186/s12866-020-01725-7
Song L, Wang J, Jia H, Kamran A, Qin Y, Liu Y, Hao K, Han F, Zhang C, Li B et al (2020b) An Overview of the Molecular Genetics of Plant Resistance to the Verticillium Wilt Pathogen Verticillium dahliae. Int J Mol Sci 21:1120. https://doi.org/10.3390/ijms21031120
Stintzi A, Heitz T, Prasad V, Wiedemann-Merdinoglu S, Kauffmann S, Geoffroy P, Legrand M, Fritig B (1993) Plant ‘pathogenesis-related’ proteins and their role in defense against pathogens. Biochimie 75:687–706. https://doi.org/10.1016/0300-9084(93)90100-7
Suraby EJ, Prasath D, Babu KN, Anandaraj M (2020) Identification of resistance gene analogs involved in Phytophthora capsici recognition in black pepper (Piper nigrum L.). J Plant Pathol 102:1121–1131. https://doi.org/10.1007/s42161-020-00586-3
Tavares F, Santos CL, Sellstedt A (2007) Reactive oxygen species in legume and actinorhizal nitrogen-fixing symbioses: the microsymbiont’s responses to an unfriendly reception. Physiol Plant 130:344–356. https://doi.org/10.1111/j.1399-3054.2007.00933.x
Tellis M, Mathur M, Gurjar G, Kadoo N, Gupta V (2017) Identification and functionality prediction of pathogenesis-related protein 1 from legume family. Proteins: Struct Funct Bioinformatics 85:2066–2080. https://doi.org/10.1002/prot.25361
Terras FRG, Goderis IJ, Van Leuven F, Vanderleyden J, Cammue BPA, Broekaert WF (1992) In Vitro Antifungal Activity of a Radish (Raphanus sativus L.) Seed Protein Homologous to Nonspecific Lipid Transfer Proteins 1. Plant Physiol 100:1055–1058. https://doi.org/10.1104/pp.100.2.1055
Thatcher LF, Williams AH, Garg G, Buck SAG, Singh KB (2016) Transcriptome analysis of the fungal pathogen Fusarium oxysporum f. sp. medicaginis during colonisation of resistant and susceptible Medicago truncatula hosts identifies differential pathogenicity profiles and novel candidate effectors. BMC Genomics 17:860. https://doi.org/10.1186/s12864-016-3192-2
Thomma BP, Cammue BP, Thevissen K (2002) Plant defensins. Planta 216:193–202. https://doi.org/10.1007/s00425-002-0902-6
van der Hoorn RAL, Kamoun S (2008) From Guard to Decoy: A New Model for Perception of Plant Pathogen Effectors. Plant Cell 20:2009–2017. https://doi.org/10.1105/tpc.108.060194
van Loon LC, Geraats BPJ, Linthorst HJM (2006) Ethylene as a modulator of disease resistance in plants. Trends Plant Sci 11:184–191. https://doi.org/10.1016/j.tplants.2006.02.005
Vega-Sánchez ME, Redinbaugh MG, Costanzo S, Dorrance AE (2005) Spatial and temporal expression analysis of defense-related genes in soybean cultivars with different levels of partial resistance to Phytophthora sojae. Physiol Mol Plant Pathol 66:175–182. https://doi.org/10.1016/j.pmpp.2005.07.001
Venisse J-S, Malnoy M, Faize M, Paulin J-P, Brisset M-N (2002) Modulation of defense responses of malus spp. during compatible and incompatible interactions with Erwinia amylovora. Mol Plant Microbe Interact 15:1204–1212. https://doi.org/10.1094/MPMI.2002.15.12.1204
Vergnes S, Gayrard D, Veyssière M, Toulotte J, Martinez Y, Dumont V, Bouchez O, Rey T, Dumas B (2020) Phyllosphere Colonization by a Soil Streptomyces sp. Promotes Plant Defense Responses Against Fungal Infection. MPMI 33:223–234. https://doi.org/10.1094/MPMI-05-19-0142-R
Vergnes S, Ladouce N, Fournier S, Ferhout H, Attia F, Dumas B (2014) Foliar treatments with Gaultheria procumbens essential oil induce defense responses and resistance against a fungal pathogen in Arabidopsis. Front Plant Sci 5:477. https://doi.org/10.3389/fpls.2014.00477
Vlot AC, Klessig DF, Park S-W (2008) Systemic acquired resistance: the elusive signal(s). Curr Opin Plant Biol 11:436–442. https://doi.org/10.1016/j.pbi.2008.05.003
Wall LG, Berry AM (2008) Early Interactions, Infection And Nodulation In Actinorhizal Symbiosis. In: Pawlowski K, Newton WE (eds) Nitrogen-fixing Actinorhizal Symbioses. Springer, Netherlands, Dordrecht, pp 147–166
Wei Z-M, Laby RJ, Zumoff CH, Bauer DW, He SY, Collmer A, Beer SV (1992) Harpin, Elicitor of the Hypersensitive Response Produced by the Plant Pathogen Erwinia amylovora. Science 257:85–88. https://doi.org/10.1126/science.1621099
Yang C-L, Liang S, Wang H-Y, Han L-B, Wang F-X, Cheng H-Q, Wu X-M, Qu Z-L, Wu J-H, Xia G-X (2015) Cotton Major Latex Protein 28 Functions as a Positive Regulator of the Ethylene Responsive Factor 6 in Defense against Verticillium dahliae. Mol Plant 8:399–411. https://doi.org/10.1016/j.molp.2014.11.023
Xiang S, Wu S, Zhang H, Mou M, Chen Y, Li D, Wang H, Chen L, Yu D (2020) The PIFs redundantly control plant defense response against Botrytis cinerea in Arabidopsis. Plants 9:1246. https://doi.org/10.3390/plants9091246
Yamaguchi Y, Huffaker A, Bryan AC, Tax FE, Ryan CA (2010) PEPR2 is a second receptor for the Pep1 and Pep2 peptides and contributes to defense responses in arabidopsis. Plant Cell 22:508–522. https://doi.org/10.1105/tpc.109.068874
Yu H, Bao H, Zhang Z, Cao Y (2019) Immune Signaling Pathway during Terminal Bacteroid Differentiation in Nodules. Trends Plant Sci 24:299–302. https://doi.org/10.1016/j.tplants.2019.01.010
Yu H, Xiao A, Dong R, Fan Y, Zhang X, Liu C, Wang C, Zhu H, Duanmu D, Cao Y et al (2018) Suppression of innate immunity mediated by the CDPK-Rboh complex is required for rhizobial colonization in Medicago truncatula nodules. New Phytol 220:425–434. https://doi.org/10.1111/nph.15410
Zeng L, Chen H, Wang Y, Hicks D, Ke H, Pruneda-Paz J, Dehesh K (2022) ORA47 is a transcriptional regulator of a general stress response hub. Plant J 110:562–571. https://doi.org/10.1111/tpj.15688
Zeng T, Rodriguez-Moreno L, Mansurkhodzaev A, Wang P, van den Berg W, Gasciolli V, Cottaz S, Fort S, Thomma BPHJ, Bono JJ et al (2020) A lysin motif effector subverts chitin-triggered immunity to facilitate arbuscular mycorrhizal symbiosis. New Phytol 225:448–460. https://doi.org/10.1111/nph.16245
Zhang N, Li R, Shen W, Jiao S, Zhang J, Xu W (2018) Genome-wide evolutionary characterization and expression analyses of major latex protein (MLP) family genes in Vitis vinifera. Mol Genet Genomics 293:1061–1075. https://doi.org/10.1007/s00438-018-1440-7
Zhao S, Qi X (2008) Signaling in Plant Disease Resistance and Symbiosis. J Integr Plant Biol 50:799–807. https://doi.org/10.1111/j.1744-7909.2008.00702.x
Zeng L, Velásquez AC, Munkvold KR, Zhang J, Martin GB (2012) A tomato LysM receptor-like kinase promotes immunity and its kinase activity is inhibited by AvrPtoB. Plant J 69:92–103. https://doi.org/10.1111/j.1365-313X.2011.04773.x
Zipfel C, Oldroyd GED (2017) Plant signalling in symbiosis and immunity. Nature 543:328–336. https://doi.org/10.1038/nature22009
Zhou T, Xu W, Hirani AH, Liu Z, Tuan PA, Ayele BT, Daayf F, McVetty PBE, Duncan RW, Li G (2019) Transcriptional insight into Brassica napus resistance genes LepR3 and Rlm2-mediated defense response against the leptosphaeria maculans infection. Front Plant Sci 10
Acknowledgements
M. Vincent is granted a doctoral fellowship by the Ministry of Higher Education and Research (MESR, France). This review is part of a project supported by the French National program EC2CO (Ecosphère Continentale et Côtière). The authors thank Benjamin Gourion (Laboratoire des Interactions Plantes—Microbes—Environnement—Université Toulouse III Paul Sabatier, CNRS) for his advices and Cyril Libourel (Laboratoire de Recherche en Sciences Végétales—Université Toulouse III Paul Sabatier, CNRS) for his help in researching orthologs of defence genes in the Medicago truncatula genome.
Author information
Authors and Affiliations
Contributions
VM, BH, HAE and HBA conceptualised the review. VM generated the bibliography atlas of plant defence genes in pathogenic and symbiotic models, and conducted A. glutinosa transcriptomic and genomic data exploration with the help of BH and GM. VM and HBA wrote the manuscript with all authors' contributions.
Corresponding author
Additional information
Publisher's note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Vincent, M., Boubakri, H., Gasser, M. et al. What contribution of plant immune responses in Alnus glutinosa-Frankia symbiotic interactions?. Symbiosis 89, 27–52 (2023). https://doi.org/10.1007/s13199-022-00889-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s13199-022-00889-2