Artículo

Ibáñez, F.; Wall, L.; Fabra, A."Starting points in plant-bacteria nitrogen-fxing symbioses: Intercellular invasion of the roots" (2017) Journal of Experimental Botany. 68(8):1905-1918
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Abstract:

Agricultural practices contribute to climate change by releasing greenhouse gases such as nitrous oxide that are mainly derived from nitrogen fertilizers. Therefore, understanding biological nitrogen fxation in farming systems is benefcial to agriculture and environmental preservation. In this context, a better grasp of nitrogen-fxing systems and nitrogen-fxing bacteria-plant associations will contribute to the optimization of these biological processes. Legumes and actinorhizal plants can engage in a symbiotic interaction with nitrogen-fxing rhizobia or actinomycetes, resulting in the formation of specialized root nodules. The legume-rhizobia interaction is mediated by a complex molecular signal exchange, where recognition of different bacterial determinants activates the nodulation program in the plant. To invade plants roots, bacteria follow different routes, which are determined by the host plant. Entrance via root hairs is probably the best understood. Alternatively, entry via intercellular invasion has been observed in many legumes. Although there are common features shared by intercellular infection mechanisms, differences are observed in the site of root invasion and bacterial spread on the cortex reaching and infecting a susceptible cell to form a nodule. This review focuses on intercellular bacterial invasion of roots observed in the Fabaceae and considers, within an evolutionary context, the different variants, distribution and molecular determinants involved. Intercellular invasion of actinorhizal plants and Parasponia is also discussed. © 2016 The Author.

Registro:

Documento: Artículo
Título:Starting points in plant-bacteria nitrogen-fxing symbioses: Intercellular invasion of the roots
Autor:Ibáñez, F.; Wall, L.; Fabra, A.
Filiación:Departamento de Ciencias Naturales, Facultad de Ciencias Exactas Físico-Químicas y Naturales, Universidad Nacional de Río Cuarto, Río Cuarto, Córdoba, Argentina
Departamento de Ciencia y Tecnología, Universidad Nacional de Quilmes, Bernal, Buenos Aires, Argentina
Palabras clave:Actinorhizal plants; Intercellular invasion; Legumes; Molecular signaling; Rhizobia; Symbioses
Año:2017
Volumen:68
Número:8
Página de inicio:1905
Página de fin:1918
DOI: http://dx.doi.org/10.1093/jxb/erw387
Handle:http://hdl.handle.net/20.500.12110/paper_00220957_v68_n8_p1905_Ibanez
Título revista:Journal of Experimental Botany
Título revista abreviado:J. Exp. Bot.
ISSN:00220957
CODEN:JEBOA
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_00220957_v68_n8_p1905_Ibanez

Referencias:

  • Allen, O.N., Allen, E.K., (1981) The Leguminosae: A Source Book of Characteristics, Uses and Nodulation, , University of Wisconsin Press: Madison, WI/Macmillan Publishing, London
  • Beauchemin, N.J., Furnholm, T., Lavenus, J., Svistoonoff, S., Doumas, P., Bogusz, D., Laplaze, L., Tisa, L.S., Casuarina root exudates alter the physiology, surface properties, and plant infectivity of Frankia sp. Strain CcI3 (2012) Applied and Environmental Microbiology, 78, pp. 575-580
  • Bender, G.L., Nayudu, M., Goydych, W., Rolfe, B.G., Early infection events in the nodulation of the non-legume Parasponia andersonii by Bradyrhizobium (1987) Plant Science, 51, pp. 285-293
  • Berg, R.H., Frankia forms infection threads (1999) Canadian Journal of Botany, 77, pp. 1327-1333
  • Berg, R.H., Cytoplasmic bridge formation in the nodule apex of actinorhizal root nodules (1999) Canadian Journal of Botany, 77, pp. 1351-1357
  • Bhuvaneswari, T.V., Turgeon, B.G., Bauer, W.D., Early events in the infection of soybean (Glycine max [L.] Merr.) by Rhizobium japonicum. I. Localization of infectible root cells (1980) Plant Physiology, 66, pp. 1027-1031
  • Bonaldi, K., Gourion, B., Fardoux, J., Large-scale transposon mutagenesis of photosynthetic Bradyrhizobium sp. Strain ORS278 reveals new genetic loci putatively important for nod-independent symbiosis with Aeschynomene indica (2010) Molecular Plant-Microbe Interactions, 23, pp. 760-770
  • Bonaldi, K., Gargani, D., Prin, Y., Fardoux, J., Gully, D., Nouwen, N., Goormachtig, S., Giraud, E., Nodulation of Aeschynomene afraspera and A. Indica by photosynthetic Bradyrhizobium Sp. Strain ORS285: The nod-dependent versus the nod-independent symbiotic interaction (2011) Molecular Plant-Microbe Interactions, 11, pp. 1359-1371
  • Boogerd, F.C., Van Rossum, D., Nodulation of groundnut by Bradyrhizobium: A simple infection process by crack entry (1997) FEMS Microbiology Reviews, 21, pp. 5-27
  • Bryan, J.A., Berlyn, G.P., Gordon, J.C., Towards a new concept of the evolution of symbiotic nitrogen fxation in the Leguminosae (1995) Plant and Soil, 186, pp. 151-159
  • Cannon, S.B., McKain, M.R., Harkess, A., Multiple polyploidy events in the early radiation of nodulating and nonnodulating legumes (2015) Molecular Biology and Evolution, 32, pp. 193-210
  • Capoen, W., Den Herder, J., Sun, J., Verplancke, C., De Keyser, A., De Rycke, R., Goormachtig, S., Holsters, M., Calcium spiking patterns and the role of the calcium/calmodulin-dependent kinase CCaMK in lateral root base nodulation of Sesbania rostrata (2009) Plant Cell, 21, pp. 1526-1540
  • Capoen, W., Oldroyd, G., Goormachtig, S., Sesbania rostrata: A case study of natural variation in legume nodulation (2010) New Phytologist, 186, pp. 340-345
  • Cérémonie, H., Debellé, F., Fernandez, M.P., Structural and functional comparison of Frankia root hair deforming factor and rhizobia Nod factor (1999) Canadian Journal of Botany, 77, pp. 1293-1301
  • Chandler, M.R., Some observations on infection of Arachis hypogaea L. By rhizobium (1978) Journal of Experimental Botany, 29, pp. 749-755
  • Chandler, M.R., Date, R.A., Roughley, R.J., Infection and root-nodule development in Stylosanthes species by rhizobium (1982) Journal of Experimental Botany, 33, pp. 47-57
  • Charpentier, M., Oldroyd, G., How close are we to nitrogen-fxing cereals? (2010) Current Opinion in Plant Biology, 31, pp. 556-564
  • Chen, C., Zhu, H., Are common symbiosis genes required for endophytic rice-rhizobial interactions? (2013) Plant Signaling and Behaviour, 89, p. e25453
  • Chi, F., Shen, S.H., Cheng, H.P., Jing, Y.X., Yanni, Y.G., Dazzo, F.B., Ascending migration of endophytic rhizobia, from roots to leaves, inside rice plants and assessment of benefts to rice growth physiology (2005) Applied and Environmental Microbiology, 71, pp. 7271-7278
  • Clavijo, F., Diedhiou, I., Vaissayre, V., The Casuarina NIN gene is transcriptionally activated throughout Frankia root infection as well as in response to bacterial diffusible signals (2015) New Phytologist, 208, pp. 887-903
  • De Faria, S., Hay, G., Sprent, J., Entry of rhizobia into roots of Mimosa scabrella Bentham occurs between epidermal cells (1988) Journal of General Microbiology, 134, pp. 2291-2296
  • Delaux, P.M., Radhakrishnan, G., Oldroyd, G., Tracing the evolutionary path to nitrogen-fxing crops (2015) Current Opinion in Plant Biology, 26, pp. 95-99
  • Delaux, P.M., Radhakrishnan, G.V., Jayaraman, D., Algal ancestor of land plants was preadapted for symbiosis (2015) Proceedings of the National Academy of Sciences, USA, 112, pp. 13390-13395
  • D'Haeze, W., Gao, M., De Rycke, R., Van Montagu, M., Engler, G., Holsters, M., Roles for azorhizobial Nod factors and surface polysaccharides in intercellular invasion and nodule penetration, respectively (1998) Molecular Plant-Microbe Interactions, 11, pp. 999-1008
  • D'Haeze, W., Mergaert, P., Promé, J.C., Holsters, M., Nod factor requirements for effcient stem and root nodulation of the tropical legume Sesbania rostrata (2000) Journal of Biological Chemistry, 275, pp. 15676-15684
  • D'Haeze, W., De Rycke, R., Mathis, R., Goormachtig, S., Pagnotta, S., Verplancke, C., Capoen, W., Holsters, M., Reactive oxygen species and ethylene play a positive role in lateral root base nodulation of a semiaquatic legume (2003) Proceedings of the National Academy of Sciences USA, 100, pp. 11789-11794
  • Doyle, J., Phylogenetic perspectives on the origins of nodulation (2011) Molecular Plant-Microbe Interactions, 24, pp. 1289-1295
  • Frugier, F., Kosuta, S., Murray, J.D., Crespi, M., Szczyglowski, K., Cytokinin: Secret agent of symbiosis (2008) Trends in Plant Science, 13, pp. 115-120
  • Gabbarini, L., Wall, L., Analysis of nodulation kinetics in Frankia-Discaria trinervis symbiosis reveals different factors involved in the nodulation process (2008) Physiologia Plantarum, 133, pp. 776-785
  • Gage, D.J., Infection and invasion of roots by symbiotic, nitrogen-fxing rhizobia during nodulation of temperate legumes (2004) Microbiology and Molecular Biology Reviews, 68, pp. 280-300
  • Gherbi, H., Markmann, K., Svistoonoff, S., Estevan, J., Autran, D., Giczey, G., SymRK defnes a common genetic basis for plant root endosymbioses with arbuscular mycorrhiza fungi, rhizobia, and Frankia bacteria (2008) Proceedings of the National Academy of Sciences, USA, 105, pp. 4928-4932
  • Giraud, E., Moulin, L., Vallenet, D., Barbe, V., Cytryn, E., Avarre, J.C., Legumes symbioses: Absence of Nod genes in photosynthetic bradyrhizobia (2007) Science, 316, pp. 1307-1312
  • González-Sama, A., Lucas, M.M., De Felipe, M.R., Pueyo, J.J., An unusual infection mechanism and nodule morphogenesis in white lupin (Lupinus albus) (2004) New Phytologist, 163, pp. 371-380
  • Goormachtig, S., Capoen, W., Holsters, M., Rhizobium infection: Lessons from the versatile nodulation behaviour of water-tolerant legumes (2004) Trends in Plant Science, 9, pp. 518-522
  • Goormachtig, S., Capoen, W., James, E.K., Holsters, M., Switch from intracellular to intercellular invasion during water stress-tolerant legume nodulation (2004) Proceedings of the National Academy of Sciences, USA, 101, pp. 6303-6308
  • Granqvist, E., Sun, J., Op Den Camp, R., Pujic, P., Hill, L., Normand, P., Bacterial-induced calcium oscillations are common to nitrogen-fxing associations of nodulating legumes and nonlegumes (2015) New Phytologist, 207, pp. 551-558
  • Guha, S., Sarkar, M., Ganguly, P., Uddin, M.R., Mandal, S., DasGupta, M., Segregation of nod-containing and nod-defcient bradyrhizobia as endosymbionts of Arachis hypogaea and as endophytes of Oryza sativa in intercropped felds of Bengal Basin, India (2016) Environmental Microbiology, 18, pp. 2575-2590
  • Hayashi, T., Shimoda, Y., Sato, S., Tabata, S., Imaizumi-Anraku, H., Hayashi, M., Rhizobial infection does not require cortical expression of upstream common symbiosis genes responsible for the induction of Ca2+ spiking (2014) Plant Journal, 77, pp. 146-159
  • Hirsch, A.M., Developmental biology of legume nodulation (1992) New Phytologist, 122, pp. 211-237
  • Hirsch, A.M., Yu, N., Ma, N., Schwartz, A.R., De Hoff, P.L., The Chamaecrista fasciculata nitrogen-fxing symbiosis (2009) Botany and Mycology 2009 Abstract 446, , http://www.2009.botanyconference.org/engine/search/index.php?func=detail&aid=446, (September 30, 2009)
  • Ibáñez, F., Angelini, J., Figueredo, M.S., Muñoz, V., Tonelli, M.L., Fabra, A., Sequence and expression analysis of putative Arachis hypogaea (peanut) Nod factor perception proteins (2015) Journal of Plant Research, 128, pp. 709-718
  • Ibáñez, F., Fabra, A., Rhizobial Nod factors are required for cortical cell division in the nodule morphogenetic programme of the Aeschynomeneae legume Arachis (2011) Plant Biology, 13, pp. 794-800
  • Imanishi, L., (2015) Bases Comunes de la Simbiosis Actinorrícica: Análisis Comparativo Entre Discaria Trinervis y Casuarina Glauca, , PhD thesis, Universidad Nacional de Quilmes
  • James, E., Sprent, J., Development of N2-fxing nodules on the wetland legume Lotus uliginosus exposed to conditions of fooding (1999) New Phytologist, 142, pp. 219-231
  • James, E.K., Sprent, J.I., Sutherland, J.M., McInroy, S.G., Minchin, F.R., The structure of nitrogen fxing root nodules on the aquatic Mimosoid legume Neptunia plena (1992) Annals of Botany, 69, pp. 173-180
  • Kaku, H., Nishizawa, Y., Ishii-Minami, N., Akimoto-Tomiyama, C., Dohmae, N., Takio, K., Minami, E., Shibuya, N., Plant cells recognize chitin fragments for defense signaling through a plasma membrane receptor (2006) Proceedings of the National Academy of Sciences, USA, 103, pp. 11086-11091
  • Karas, B., Murray, J., Gorzelak, M., Smith, A., Sato, S., Tabata, S., Szczyglowski, K., Invasion of Lotus japonicus root hairless 1 by Mesorhizobium loti involves the nodulation factor-dependent induction of root hairs (2005) Plant Physiology, 137, pp. 1331-1344
  • Kawaharada, Y., Kelly, S., Nielsen, M.W., Hjuler, C.T., Gysel, K., Muszynski, A., Receptor-mediated exopolysaccharide perception controls bacterial infection (2015) Nature, 523, pp. 308-312
  • Liang, Y., Cao, Y., Tanaka, K., Thibivilliers, S., Wan, J., Choi, J., Kang, C.H., Stacey, G., Nonlegumes respond to rhizobial Nod factors by suppressing the innate immune response (2013) Science, 341, pp. 1384-1387
  • Lievens, S., Goormachtig, S., Den Herder, J., Capoen, W., Mathis, R., Hedden, P., Holsters, M., Gibberellins are involved in nodulation of Sesbania rostrata (2005) Plant Physiology, 139, pp. 1366-1379
  • Liu, Q., Berry, A.M., The infection process and nodule initiation in the Frankia-Ceanothus root nodule symbiosis (1991) Protoplasma, 163, pp. 82-92
  • Madsen, L.H., Tirichine, L., Jurkiewicz, A., Sullivan, J.T., Heckmann, A.B., Bek, A.S., The molecular network governing nodule organogenesis and infection in the model legume Lotus japonicus (2010) Nature Communications, 1, pp. 1-12
  • Maillet, F., Poinsot, V., André, O., Puech-Pagès, V., Haouy, A., Gueunier, M., Fungal lipochitooligosaccharide symbiotic signals in arbuscular mycorrhiza (2011) Nature, 469, pp. 58-63
  • Markmann, K., Parniske, M., (2009) Evolution of Root Endosymbiosis with Bacteria: How Novel Are Nodules? Trends in Plant Science, 14, pp. 77-86
  • Marvel, D.J., Torrey, J.G., Ausubel, F.M., Rhizobium symbiotic genes required for nodulation of legume and nonlegume hosts (1987) Proceedings of the National Academy of Sciences, USA, 84, pp. 1319-1323
  • Mathesius, U., Weinman, J.J., Rolfe, B.G., Djordjevic, M.A., Rhizobia can induce nodules in white clover by 'hijacking' mature cortical cells activated during lateral root development (2000) Molecular Plant-Microbe Interactions, 13, pp. 170-182
  • Mithöfer, A., Suppression of plant defense in rhizobia-legume symbiosis (2002) Trends in Plant Science, 7, pp. 440-444
  • Morgante, C., Castro, S., Fabra, A., Role of rhizobial EPS in the evasion of peanut defense response during the crack-entry infection process (2007) Soil Biology and Biochemistry, 39, pp. 1222-1225
  • Naisbitt, T., James, E.K., Sprent, J.I., The evolutionary signifcance of the legume genus Chamaecrista, as determined by nodule structure (1992) New Phytologist, 122, pp. 487-492
  • Okazaki, S., Kaneko, T., Sato, S., Saeki, K., Hijacking of leguminous nodulation signaling by the rhizobial type III secretion system (2013) Proceedings of the National Academy of Sciences, USA, 110, pp. 17131-21736
  • Okazaki, S., Tittabutr, P., Teulet, A., Rhizobium-legume symbiosis in the absence of Nod factors: Two possible scenarios with or without the T3SS (2015) The ISME Journal, 1-11
  • Oldroyd, G., Dissecting symbiosis: Developments in Nod factor signal transduction (2001) Annals of Botany, 87, pp. 709-718
  • Oldroyd, G., Speak, friend, and enter: Signaling systems that promote benefcial symbiotic associations in plants (2013) Nature Reviews Microbiology, 11, pp. 252-263
  • Op Den Camp, R., Streng, A., De Mita, S., Cao, Q., Polone, E., Liu, W., LysM-type mycorrhizal receptor recruited for Rhizobium symbiosis in nonlegume Parasponia (2011) Science, 331, pp. 909-912
  • Parniske, M., Arbuscular mycorrhiza: The mother of plant root endosymbioses (2008) Nature Reviews Microbiology, 6, pp. 763-775
  • Pawlowski, K., Demchenko, K.N., The diversity of actinorhizal symbiosis (2012) Protoplasma, 249, pp. 967-979
  • Perrine-Walker, F.M., Prayitno, J., Rolfe, B.G., Weinman, J.J., Hocart, C.H., Infection process and the interaction of rice roots with rhizobia (2007) Journal of Experimental Botany, 58, pp. 3343-3350
  • Podlešáková, K., Fardoux, J., Patrel, D., Bonaldi, K., Novák, O., Strnad, M., Giraud, E., Nouwen, N., Rhizobial synthesized cytokinins contribute to but are not essential for the symbiotic interaction between photosynthetic Bradyrhizobia and Aeschynomene legumes (2013) Molecular Plant-Microbe Interactions, 26, pp. 1232-1238
  • Ranga Rao, V., Effect of root temperature on the infection processes and nodulation in Lotus and Stylosanthes (1977) Journal of Experimental Botany, 28, pp. 241-259
  • Renier, A., Maillet, F., Fardoux, J., Poinsot, V., Giraud, E., Nouwen, N., Photosynthetic Bradyrhizobium sp. Strain ORS285 synthesizes 2-O-methylfucosylated lipochitooligosaccharides for nod gene-dependent interaction with Aeschynomene plants (2011) Molecular Plant-Microbe Interactions, 24, pp. 1440-1447
  • Rogers, C., Oldroyd, G.E., Synthetic biology approaches to engineering the nitrogen symbiosis in cereals (2014) Journal of Experimental Botany, 65, pp. 1939-1946
  • Rolfe, B.G., Gresshoff, P.M., Genetic analysis of legume nodule initiation (1988) Annual Review of Plant Physiology and Plant Molecular Biology, 39, pp. 297-319
  • Saha, S., Paul, A., Herring, L., Dutta, A., Bhattacharya, A., Samaddar, S., Goshe, M.B., DasGupta, M., Gatekeeper tyrosine phosphorylation of SYMRK is essential for synchronizing the epidermal and cortical responses in root nodule symbiosis (2016) Plant Physiology, 171, pp. 71-81
  • Sinharoy, S., DasGupta, M., RNA interference highlights the role of CCaMK in dissemination of endosymbionts in the Aeschynomeneae legume Arachis (2009) Molecular Plant-Microbe Interactions, 22, pp. 1466-1475
  • Soltis, D.E., Soltis, P.S., Morgan, D.R., Swensen, S.M., Mullin, B.C., Dowd, J.M., Martin, P.G., Chloroplast gene sequence data suggest a single origin of the predisposition for symbiotic nitrogen fxation in angiosperms (1995) Proceedings of the National Academy of Sciences, USA, 92, pp. 2647-9651
  • Soyano, T., Hayashi, M., Transcriptional networks leading to symbiotic nodule organogenesis (2014) Current Opinion in Plant Biology, 20, pp. 146-154
  • Sprent, J.I., Which steps are essential for the formation of functional legume nodules? (1989) New Phytologist, 111, pp. 129-153
  • Sprent, J.I., James, E., Legume evolution: Where do nodules and mycorrhizas ft in? (2007) Plant Physiology, 144, pp. 575-581
  • Sprent, J.I., Evolving ideas of legume evolution and diversity: A taxonomic perspective on the occurrence of nodulation (2007) New Phytologist, 174, pp. 11-25
  • Sprent, J.I., 60Ma of legume nodulation. What's new? What's changing? (2008) Journal of Experimental Botany, 59, pp. 1081-1084
  • Subba-Rao, N.S., Mateos, P.F., Baker, D., Stuart Pankratz, H., Palma, J., Dazzo, F., Sprent, J.I., The unique root-nodule symbiosis between Rhizobium and the aquatic legume, Neptunia natans (L.f.) Druce (1995) Planta, 196, pp. 311-320
  • Svistoonoff, S., Benabdoun, F.M., Nambiar-Veetil, M., Imanishi, L., Vaissayre, V., Cesari, S., The independent acquisition of plant root nitrogen-fxing symbiosis in fabids recruited the same genetic pathway for nodule organogenesis (2013) PLoS One, 8, p. e64515
  • Svistoonoff, S., Laplaze, L., Auguy, F., Runions, J., Duponnois, R., Haseloff, J., Franche, C., Bogusz, D., Cg12 expression is specifcally linked to infection of root hairs and cortical cells during Casuarina glauca and Allocasuarina verticillata actinorhizal nodule development (2003) Molecular Plant-Microbe Interactions, 16, pp. 600-607
  • Svistoonoff, S., Valerie, H., Gherbi, H., Actinorhizal root nodule symbioses: What is signaling telling on the origins of nodulation? (2014) Current Opinion in Plant Biology, 20, pp. 11-18
  • Trinick, M.J., Symbiosis between Rhizobium and the non-legume, Trema aspera (1973) Nature, 244, pp. 459-460
  • Trinick, M.J., Galbraith, J., The Rhizobium requirements of the non-legume Parasponia in relationship to the cross-inoculation group concept of legumes (1980) New Phytologist, 86, pp. 17-26
  • Uheda, E., Daimon, H., Yoshizako, F., Colonization and invasion of peanut (Arachis hypogaea L.) roots by gusA-marked Bradyrhizobium sp (2001) Canadian Journal of Botany, 79, pp. 733-738
  • Valverde, C., Wall, L.G., Time course of nodule development in Discaria trinervis (Rhamnaceae)-Frankia symbiosis (1999) New Phytologist, 141, pp. 345-354
  • Valverde, C., Wall, L.G., The regulation of nodulation in Discaria trinervis (Rhamnaceae)Frankia symbiosis (1999) Canadian Journal of Botany, 77, pp. 1302-1310
  • Van Brussel, A.A., Bakhuizen, R., Van Spronsen, P.C., Spaink, H.P., Tak, T., Lugtenberg, B.J., Kijne, J.W., Induction of pre-infection thread structures in the leguminous host plant by mitogenic lipo-oligosaccharides of Rhizobium (1992) Science, 257, pp. 70-72
  • Vega-Hernández, M.C., Pérez-Galdona, R., Dazzo, F.B., Jarabo-Lorenzo, A., Alfayate, M.C., León-Barrios, M., Novel infection process in the indeterminate root nodule symbiosis between Chamaecytisus proliferus (tagasaste) and Bradyrhizobium sp (2001) New Phytologist, 150, pp. 707-721
  • Vernié, T., Kim, J., Frances, L., The NIN transcription factor coordinates diverse nodulation programs in different tissues of the Medicago truncatula root (2015) The Plant Cell, 27, pp. 3410-3424
  • Wall, L.G., The actinorhizal symbiosis (2000) Journal of Plant Growth Regulation, 19, pp. 167-182
  • Wall, L.G., Berry, A.M., Early interactions, infection and nodulation in actinorhizal symbiosis (2008) Nitrogen Fxation: Origins, Applications, and Research Progress, Vol. 6 Nitrogen-Fixing Actinorhizal Symbioses, pp. 147-166. , Pawlowski, K., Newton, W.E., eds. Springer
  • Wall, L.G., Huss-Danell, K., Regulation of nodulation in Alnus incana-Frankia symbiosis (1997) Physiologia Plantarum, 99, pp. 594-600
  • Wan, J., Zhang, X.C., Neece, D., Ramonell, K.M., Clough, S., Kim, S.Y., Stacey, M.G., Stacey, G., A LysM receptor-like kinase plays a critical role in chitin signaling and fungal resistance in Arabidopsis (2008) Plant Cell, 20, pp. 471-481
  • Wang, C., Zhu, M., Duan, L., Yu, H., Chang, X., Heng Kang, L., Lotus japonicus clathrin heavy chain 1 is associated with Rho-like GTPase ROP6 and involved in nodule formation (2015) Plant Physiology, 167, pp. 1497-1510
  • Werner, G.D., Cornwell, W.K., Sprent, J.I., Kattge, J., Kiers, E.T., A single evolutionary innovation drives the deep evolution of symbiotic N2-fxation in angiosperms (2014) Nature Communications, 5, p. 4087
  • Xie, F., Murray, J.D., Kim, J., Heckmann, A., Edwards, A., Oldroyd, G.E., Downie, J.A., Legume pectate lyase required for root infection by rhizobia (2012) Proceedings of the National Academy of Sciences, USA, 109, pp. 633-638

Citas:

---------- APA ----------
Ibáñez, F., Wall, L. & Fabra, A. (2017) . Starting points in plant-bacteria nitrogen-fxing symbioses: Intercellular invasion of the roots. Journal of Experimental Botany, 68(8), 1905-1918.
http://dx.doi.org/10.1093/jxb/erw387
---------- CHICAGO ----------
Ibáñez, F., Wall, L., Fabra, A. "Starting points in plant-bacteria nitrogen-fxing symbioses: Intercellular invasion of the roots" . Journal of Experimental Botany 68, no. 8 (2017) : 1905-1918.
http://dx.doi.org/10.1093/jxb/erw387
---------- MLA ----------
Ibáñez, F., Wall, L., Fabra, A. "Starting points in plant-bacteria nitrogen-fxing symbioses: Intercellular invasion of the roots" . Journal of Experimental Botany, vol. 68, no. 8, 2017, pp. 1905-1918.
http://dx.doi.org/10.1093/jxb/erw387
---------- VANCOUVER ----------
Ibáñez, F., Wall, L., Fabra, A. Starting points in plant-bacteria nitrogen-fxing symbioses: Intercellular invasion of the roots. J. Exp. Bot. 2017;68(8):1905-1918.
http://dx.doi.org/10.1093/jxb/erw387