Il est généralement admis que la symbiose rhizobienne a pu recruter, au cours de l'évolution, des éléments de signalisation symbiotique préexistants dans la symbiose mycorhizienne, beaucoup plus ancienne. Dans cet ensemble d'éléments qui constitue la CSP, DMI3 joue un rôle central, puisque le rôle des gènes DMI1 et DMI2 serait uniquement de permettre l'activation de DMI3 (Hayashi et al., 2010; Madsen et al., 2010). Compte tenu de la similitude des processus d'infection dans ces deux symbioses, on peut supposer que le recrutement de DMI3 pour l'infection par les rhizobia ne posait pas de difficultés d'adaptation particulières. Nos résultats montrent en effet que pour les deux types de symbiotes, DMI3 joue un rôle très similaire, en agissant de façon cellule autonome pour guider la progression de l'infection à travers les tissus racinaires. Cependant une CCaMK de riz ne permet pas de restaurer une infection normale chez un mutant dmi3 de M. truncatula, ce qui peut suggérer que l'infection par Rhizobium nécessite des propriétés particulières de la CCaMK (Godfroy et al., 2006). Une différence majeure entre les symbioses mycorhizienne et rhizobienne est que la seconde nécessite un processus d'organogénèse qui n'existe pas dans la première. Il peut donc paraître a priori surprenant que DMI3 et les autres gènes de la CSP aient également été recrutés pour l'induction du processus d'organogénèse nodulaire. Cependant ce rôle de DMI3 dans l'organogénèse ne semble pas avoir nécessité une modification importante de la protéine, puisqu'une CCaMK de riz est capable de restaurer la formation des nodosités chez un mutant
dmi3 de M. truncatula (Godfroy et al., 2006). De plus, le fait d'utiliser un même gène pour les
voies de signalisation contrôlant l'organogénèse et l'infection peut constituer un avantage pour assurer un bon couplage entre ces deux processus.
Nos résultats montrent par ailleurs que le processus d'organogénèse nodulaire requiert l'intervention de DMI3 non seulement dans différents tissus de la racine, mais également à
77 plusieurs niveaux dans la voie de signalisation, à la fois en amont et en aval du messager secondaire assurant la transmission du signal entre l'épiderme et le cortex. DMI3 semble donc occuper une place prépondérante dans le processus d'organogénèse, et il serait intéressant de savoir s'il joue également un rôle important dans d'autres types de symbioses impliquant une organogénèse nodulaire, mais pas de composés de type LCO. Ainsi chez les plantes actinorhiziennes nodulées par des souches de Frankia qui a priori ne possèdent pas les gènes nécessaires à la synthèse de LCO, l'orthologue du gène DMI2 joue néanmoins un rôle important dans la formation des nodosités (Gherbi et al., 2008), ce qui suggère que DMI3 pourrait également être impliqué dans ce processus. Par ailleurs, la récente émergence d'Aeschynomene evenia comme plante modèle pour l'étude des symbioses rhizobiennes indépendantes des facteurs Nod (Arrighi et al., 2012) devrait permettre de déterminer si ce type de symbiose implique également une CCaMK. Une telle implication ferait de la CCaMK un acteur incontournable de la mise en place des endosymbioses racinaires, et un véritable « lauréat de l’évolution ».
78
BIBLIOGRAPHIE
79
Akiyama, K., Matsuzaki, K. and Hayashi, H. (2005). Plant sesquiterpenes induce hyphal
branching in arbuscular mycorrhizal fungi. Nature 435, 824–827.
Alloisio, N., Queiroux, C., Fournier, P., Pujic, P., Normand, P., Vallenet, D., Medigue, C., Yamaura, M., Kakoi, K. and Kucho, K. (2010). The Frankia alni symbiotic
transcriptome. Mol Plant Microbe Interact 23, 593–607.
Amor, B. B., Shaw, S. L., Oldroyd, G. E., Maillet, F., Penmetsa, R. V., Cook, D., Long, S. R., Dénarié, J. and Gough, C. (2003). The NFP locus of Medicago truncatula controls
an early step of Nod factor signal transduction upstream of a rapid calcium flux and root hair deformation. Plant J 34, 495–506.
Anders, J., D, F. R. and Axel, O. P. (1996). Nitrogen metabolism of external hyphae of the
arbuscular mycorrhizal fungus Glomus intraradices. New phytologist 133, 705–712.
Andriankaja, A., Boisson-Dernier, A., Frances, L., Sauviac, L., Jauneau, A., Barker, D. G. and de Carvalho-Niebel, F. (2007). AP2-ERF transcription factors mediate Nod
factor dependent Mt ENOD11 activation in root hairs via a novel cis-regulatory motif.
Plant Cell 19, 2866–2885.
Ane, J. M., Kiss, G. B., Riely, B. K., Penmetsa, R. V., Oldroyd, G. E., Ayax, C., Levy, J., Debelle, F., Baek, J. M., Kalo, P., et al. (2004). Medicago truncatula DMI1 required for
bacterial and fungal symbioses in legumes. Science 303, 1364–1367.
Arrighi, J. F., Barre, A., Ben Amor, B., Bersoult, A., Soriano, L. C., Mirabella, R., de Carvalho-Niebel, F., Journet, E. P., Ghérardi, M., Huguet, T., et al. (2006). The
Medicago truncatula lysin [corrected] motif-receptor-like kinase gene family includes NFP and new nodule-expressed genes. Plant Physiol 142, 265–279.
Arrighi, J.-F., Cartieaux, F., Brown, S. C., Rodier-Goud, M., Boursot, M., Fardoux, J., Patrel, D., Gully, D., Fabre, S., Chaintreuil, C., et al. (2012). Aeschynomene evenia, a
model plant for studying the molecular genetics of the nod-independent rhizobium- legume symbiosis. Molecular plant-microbe interactions : MPMI 25, 851–61.
Augé, R. M. (2001). Water relations , drought and vesicular-arbuscular mycorrhizal
symbiosis. 3–42.
Balestrini, R., Hahn, M. G., Faccio, A., Mendgen, K. and Bonfante, P. (1996). Differential
Localization of Carbohydrate Epitopes in Plant Cell Walls in the Presence and Absence of Arbuscular Mycorrhizal Fungi. Plant Physiol 111, 203–213.
Bateman, A. and Bycroft, M. (2000). The structure of a LysM domain from E. coli
membrane-bound lytic murein transglycosylase D (MltD). J Mol Biol 299, 1113–1119.
Bell, C. D., Soltis, D. E. and Soltis, P. S. (2010). The age and diversification of the
angiosperms re-revisited. Am J Bot 97, 1296–1303.
Benedetto, A., Magurno, F., Bonfante, P. and Lanfranco, L. (2005). Expression profiles of
a phosphate transporter gene (GmosPT) from the endomycorrhizal fungus Glomus mosseae. Mycorrhiza 15, 620–627.
80
Bensmihen, S., de Billy, F. and Gough, C. (2011). Contribution of NFP LysM domains to
the recognition of Nod factors during the Medicago truncatula/Sinorhizobium meliloti symbiosis. PLoS One 6, e26114.
Benson, D. R. and Silvester, W. B. (1993). Biology of Frankia strains, actinomycete
symbionts of actinorhizal plants. Microbiol Rev 57, 293–319.
Besserer, A., Puech-Pagès, V., Kiefer, P., Gomez-Roldan, V., Jauneau, A., Roy, S., Portais, J. C., Roux, C., Bécard, G. and Séjalon-Delmas, N. (2006). Strigolactones
stimulate arbuscular mycorrhizal fungi by activating mitochondria. PLoS Biol 4, e226.
Besserer, A., Bécard, G., Roux, C. and Séjalon-Delmas, N. (2009). Role of mitochondria in
the response of arbuscular mycorrhizal fungi to strigolactones. Plant Signal Behav 4, 75– 77.
Bhuvaneswari, T. V., Bhagwat, A. A. and Bauer, W. D. (1981). Transient susceptibility of
root cells in four common legumes to nodulation by rhizobia. Plant Physiol 68, 1144– 1149.
Bonaldi, K., Gargani, D., Prin, Y., Fardoux, J., Gully, D., Nouwen, N., Goormachtig, S. and Giraud, E. (2011). Nodulation of Aeschynomene afraspera and A. indica by
photosynthetic Bradyrhizobium Sp. strain ORS285: the nod-dependent versus the nod- independent symbiotic interaction. Mol Plant Microbe Interact 24, 1359–1371.
Bonfante, P. and Genre, A. (2010). Mechanisms underlying beneficial plant-fungus
interactions in mycorrhizal symbiosis. Nature communications 1, 48.
Broghammer, A., Krusell, L., Blaise, M., Sauer, J., Sullivan, J. T., Maolanon, N., Vinther, M., Lorentzen, A., Madsen, E. B., Jensen, K. J., et al. (2012). Legume
receptors perceive the rhizobial lipochitin oligosaccharide signal molecules by direct binding. Proc Natl Acad Sci U S A 109, 13859–13864.
Brundrett, M. (2002). Cooevolutionof roots and mycorrhizas of land plants. New phytologist 154, 275–304.
Buchanen, B. B., Buchanan, B. B., Gruissem, W. and Jones, R. L. (2000). Biochemistry
and molecular biology of plants. American society of plant physiologists.
CY, T., Feng, G., XL, L. and FS, Z. (2004). Different effects of arbuscular mycorrhizal
fungal isolates from saline or non-saline soil on salinity tolerance of plants. Applied Soil
Ecology 26, 143–148.
Caetano-Anollés, G., Crist-Estes, D. K. and Bauer, W. D. (1988). Chemotaxis of
Rhizobium meliloti to the plant flavone luteolin requires functional nodulation genes. J
Bacteriol 170, 3164–3169.
Capoen, W., Sun, J., Wysham, D., Otegui, M. S., Venkateshwaran, M., Hirsch, S., Miwa, H., Downie, J. A., Morris, R. J., Ané, J.-M., et al. (2011). Nuclear membranes control
symbiotic calcium signaling of legumes. Proceedings of the National Academy of
81
Catoira, R., Galera, C., de Billy, F., Penmetsa, R. V., Journet, E. P., Maillet, F.,
Rosenberg, C., Cook, D., Gough, C. and Denarie, J. (2000). Four genes of Medicago
truncatula controlling components of a nod factor transduction pathway. Plant Cell 12, 1647–1666.
Cerri, M. R., Frances, L., Laloum, T., Auriac, M. C., Niebel, A., Oldroyd, G. E., Barker, D. G., Fournier, J. and de Carvalho-Niebel, F. (2012). Medicago truncatula ERN
transcription factors: regulatory interplay with NSP1/NSP2 GRAS factors and expression dynamics throughout rhizobial infection. Plant Physiol.
Chabaud, M., Genre, A., Sieberer, B. J., Faccio, A., Fournier, J., Novero, M., Barker, D. G. and Bonfante, P. (2011). Arbuscular mycorrhizal hyphopodia and germinated spore
exudates trigger Ca2+ spiking in the legume and nonlegume root epidermis. New Phytol
189, 347–355.
Charpentier, M., Bredemeier, R., Wanner, G., Takeda, N., Schleiff, E. and Parniske, M.
(2008). Lotus japonicus CASTOR and POLLUX are ion channels essential for
perinuclear calcium spiking in legume root endosymbiosis. Plant Cell 20, 3467–3479.
Cook, C. E., Whichard, L. P., Turner, B., Wall, M. E. and Egley, G. H. (1966).
Germination of Witchweed (Striga lutea Lour.): Isolation and Properties of a Potent Stimulant. Science 154, 1189–1190.
Croll, D. and Sanders, I. R. (2009). Recombination in Glomus intraradices, a supposed
ancient asexual arbuscular mycorrhizal fungus. BMC Evol Biol 9, 13.
Croll, D., Giovannetti, M., Koch, A. M., Sbrana, C., Ehinger, M., Lammers, P. J. and Sanders, I. R. (2009). Nonself vegetative fusion and genetic exchange in the arbuscular
mycorrhizal fungus Glomus intraradices. New Phytol 181, 924–937.
Cui, H., Levesque, M. P., Vernoux, T., Jung, J. W., Paquette, A. J., Gallagher, K. L., Wang, J. Y., Blilou, I., Scheres, B. and Benfey, P. N. (2007). An evolutionarily
conserved mechanism delimiting SHR movement defines a single layer of endodermis in plants. Science 316, 421–425.
Delaux, P.-M., Xie, X., Timme, R. E., Puech-Pages, V., Dunand, C., Lecompte, E.,
Delwiche, C. F., Yoneyama, K., Bécard, G. and Séjalon-Delmas, N. (2012). Origin of
strigolactones in the green lineage. The New phytologist 195, 857–71.
Delves, A. C., Mathews, A., Day, D. A., Carter, A. S., Carroll, B. J. and Gresshoff, P. M.
(1986). Regulation of the soybean-Rhizobium nodule symbiosis by shoot and root factors. Plant Physiol 82, 588–590.
Den Herder, G., Yoshida, S., Antolin-Llovera, M., Ried, M. K. and Parniske, M. (2012).
Lotus japonicus E3 ligase SEVEN IN ABSENTIA4 destabilizes the symbiosis receptor- like kinase SYMRK and negatively regulates rhizobial infection. Plant Cell 24, 1691– 1707.
82
Dénarié, J., Debellé, F. and Promé, J. C. (1996). Rhizobium lipo-chitooligosaccharide
nodulation factors: signaling molecules mediating recognition and morphogenesis. Annu
Rev Biochem 65, 503–535.
Endre, G., Kereszt, A., Kevei, Z., Mihacea, S., Kalo, P. and Kiss, G. B. (2002). A receptor
kinase gene regulating symbiotic nodule development. Nature 417, 962–966.
Ezawa, T., Cavagnaro, T., Smith, S., Smith, F. and Ohtomo, R. (2004). Rapid
accumulation of polyphosphate in extradical hyphae of an arbuscular mycorrhizal fungus as revealed by biochemistry and polyphosphatekinase/luciferase system. New Phytologist
161, 387–392.
Fang, Y. and Hirsch, A. M. (1998). Studying early nodulin gene ENOD40 expression and
induction by nodulation factor and cytokinin in transgenic alfalfa. Plant Physiol 116, 53– 68.
Fellbaum, C. R., Gachomo, E. W., Beesetty, Y., Choudhari, S., Strahan, G. D., Pfeffer, P. E., Kiers, E. T. and Bücking, H. (2012). Carbon availability triggers fungal nitrogen
uptake and transport in arbuscular mycorrhizal symbiosis. Proceedings of the National
Academy of Sciences of the United States of America 109, 2666–71.
Ferguson, B. J., Ross, J. J. and Reid, J. B. (2005). Nodulation phenotypes of gibberellin and
brassinosteroid mutants of pea. Plant Physiol 138, 2396–2405.
Ferrer, J. L., Austin, M. B., Stewart Jr., C. and Noel, J. P. (2008). Structure and function
of enzymes involved in the biosynthesis of phenylpropanoids. Plant Physiol Biochem 46, 356–370.
Fisher, R. F., Egelhoff, T. T., Mulligan, J. T. and Long, S. R. (1988). Specific binding of
proteins from Rhizobium meliloti cell-free extracts containing NodD to DNA sequences upstream of inducible nodulation genes. Genes Dev 2, 282–293.
Fournier, J., Timmers, A. C., Sieberer, B. J., Jauneau, A., Chabaud, M. and Barker, D. G. (2008). Mechanism of infection thread elongation in root hairs of Medicago
truncatula and dynamic interplay with associated rhizobial colonization. Plant Physiol
148, 1985–1995.
Gage, D. J. (2004). Infection and invasion of roots by symbiotic, nitrogen-fixing rhizobia
during nodulation of temperate legumes. Microbiol Mol Biol Rev 68, 280–300.
Gaude, N., Bortfeld, S., Duensing, N., Lohse, M. and Krajinski, F. (2012). Arbuscule-
containing and non-colonized cortical cells of mycorrhizal roots undergo extensive and specific reprogramming during arbuscular mycorrhizal development. Plant J 69, 510– 528.
Gehrig, H., Schüssler, A. and Kluge, M. (1996). Geosiphon pyriforme, a fungus forming
endocytobiosis with Nostoc (cyanobacteria), is an ancestral member of the Glomales: evidence by SSU rRNA analysis. J Mol Evol 43, 71–81.
83
Genre, A., Chabaud, M., Timmers, T., Bonfante, P. and Barker, D. G. (2005). Arbuscular
mycorrhizal fungi elicit a novel intracellular apparatus in Medicago truncatula root epidermal cells before infection. Plant Cell 17, 3489–3499.
Gerdemann, J. W. and Trappe, J. M. (1974). The Endogonaceae in the Pacific Northwest.
Mycol mem 1–76.
Gherbi, H., Markmann, K., Svistoonoff, S., Estevan, J., Autran, D., Giczey, G., Auguy, F., Péret, B., Laplaze, L., Franche, C., et al. (2008). SymRK defines a common genetic
basis for plant root endosymbioses with arbuscular mycorrhiza fungi, rhizobia, and Frankiabacteria. Proceedings of the National Academy of Sciences of the United States of
America 105, 4928–32.
Gibson, K. E., Kobayashi, H. and Walker, G. C. (2008). Molecular determinants of a
symbiotic chronic infection. Annu Rev Genet 42, 413–441.
Giovannetti, M., Fortuna, P., AS, C., Morini, S. and MP, N. (2001). The occurrence of
anastomosis formation and nuclear exchange in intact arbuscular mycorrhizal networks.
New phytologist 151, 717–724.
Giraud, E., Moulin, L., Vallenet, D., Barbe, V., Cytryn, E., Avarre, J. C., Jaubert, M., Simon, D., Cartieaux, F., Prin, Y., et al. (2007). Legumes symbioses: absence of Nod
genes in photosynthetic bradyrhizobia. Science 316, 1307–1312.
Gleason, C., Chaudhuri, S., Yang, T., Munoz, A., Poovaiah, B. W. and Oldroyd, G. E.
(2006). Nodulation independent of rhizobia induced by a calcium-activated kinase lacking autoinhibition. Nature 441, 1149–1152.
Gobbato, E., Marsh, J. F., Vernie, T., Wang, E., Maillet, F., Kim, J., Miller, J. B., Sun, J., Bano, S. A., Ratet, P., et al. (2012). A GRAS-Type Transcription Factor with a
Specific Function in Mycorrhizal Signaling. Curr Biol.
Godfroy, O., Debelle, F., Timmers, T. and Rosenberg, C. (2006). A rice calcium- and
calmodulin-dependent protein kinase restores nodulation to a legume mutant. Mol Plant
Microbe Interact 19, 495–501.
Goedhart, J., Hink, M. A., Visser, A. J., Bisseling, T. and Gadella Jr., T. W. (2000). In
vivo fluorescence correlation microscopy (FCM) reveals accumulation and immobilization of Nod factors in root hair cell walls. Plant J 21, 109–119.
Gomez-Roldan, V., Fermas, S., Brewer, P. B., Puech-Pagès, V., Dun, E. A., Pillot, J. P., Letisse, F., Matusova, R., Danoun, S., Portais, J. C., et al. (2008). Strigolactone
inhibition of shoot branching. Nature 455, 189–194.
Gonzalez-Rizzo, S., Crespi, M. and Frugier, F. (2006). The Medicago truncatula CRE1
cytokinin receptor regulates lateral root development and early symbiotic interaction with Sinorhizobium meliloti. Plant Cell 18, 2680–2693.
84
Goormachtig, S., Capoen, W. and Holsters, M. (2004). Rhizobium infection: lessons from
the versatile nodulation behaviour of water-tolerant legumes. Trends Plant Sci 9, 518– 522.
Gough, C. and Cullimore, J. (2011). Lipo-chitooligosaccharide signaling in endosymbiotic
plant-microbe interactions. Mol Plant Microbe Interact 24, 867–878.
Govindarajulu, M., Pfeffer, P. E., Jin, H., Abubaker, J., Douds, D. D., Allen, J. W., Bücking, H., Lammers, P. J. and Shachar-Hill, Y. (2005). Nitrogen transfer in the
arbuscular mycorrhizal symbiosis. Nature 435, 819–23.
Groth, M., Takeda, N., Perry, J., Uchida, H., Draxl, S., Brachmann, A., Sato, S., Tabata, S., Kawaguchi, M., Wang, T. L., et al. (2010). NENA, a Lotus japonicus homolog of
Sec13, is required for rhizodermal infection by arbuscular mycorrhiza fungi and rhizobia but dispensable for cortical endosymbiotic development. Plant Cell 22, 2509–2526.
Guether, M., Neuhauser, B., Balestrini, R., Dynowski, M., Ludewig, U. and Bonfante, P.
(2009). A mycorrhizal-specific ammonium transporter from Lotus japonicus acquires nitrogen released by arbuscular mycorrhizal fungi. Plant Physiol 150, 73–83.
Gust, A. A., Willmann, R., Desaki, Y., Grabherr, H. M. and Nurnberger, T. (2012). Plant
LysM proteins: modules mediating symbiosis and immunity. Trends Plant Sci 17, 495– 502.
Gutjahr, C., Banba, M., Croset, V., An, K., Miyao, A., An, G., Hirochika, H., Imaizumi- Anraku, H. and Paszkowski, U. (2008). Arbuscular mycorrhiza-specific signaling in
rice transcends the common symbiosis signaling pathway. Plant Cell 20, 2989–3005.
Haag, A. F., Arnold, M. F. F., Myka, K. K., Kerscher, B., Dall’angelo, S., Zanda, M., Mergaert, P. and Ferguson, G. P. (2012). Molecular insights into bacteroid
development during Rhizobium-legume symbiosis. FEMS microbiology reviews.
Halary, S., Malik, S.-B., Lildhar, L., Slamovits, C. H., Hijri, M. and Corradi, N. (2011).
Conserved meiotic machinery in Glomus spp., a putatively ancient asexual fungal lineage. Genome biology and evolution 3, 950–8.
Haney, C. H., Riely, B. K., Tricoli, D. M., Cook, D. R., Ehrhardt, D. W. and Long, S. R.
(2011). Symbiotic rhizobia bacteria trigger a change in localization and dynamics of the Medicago truncatula receptor kinase LYK3. Plant Cell 23, 2774–2787.
Harley, E. and Harley, J. (1987). A check-list of mycorrhiza in the British flora. New Phytol 105, 1–102.
Harrison, M. J. and van Buuren, M. L. (1995). A phosphate transporter from the
mycorrhizal fungus Glomus versiforme. Nature 378, 626–629.
Harrison, M. J., Dewbre, G. R. and Liu, J. (2002). A phosphate transporter from Medicago
truncatula involved in the acquisition of phosphate released by arbuscular mycorrhizal fungi. Plant Cell 14, 2413–2429.
85
Hayashi, T., Banba, M., Shimoda, Y., Kouchi, H., Hayashi, M. and Imaizumi-Anraku, H. (2010). A dominant function of CCaMK in intracellular accommodation of bacterial
and fungal endosymbionts. Plant J 63, 141–154.
Heckmann, A. B., Lombardo, F., Miwa, H., Perry, J. A., Bunnewell, S., Parniske, M., Wang, T. L. and Downie, J. A. (2006). Lotus japonicus nodulation requires two GRAS
domain regulators, one of which is functionally conserved in a non-legume. Plant
Physiol 142, 1739–1750.
Heidstra, R., Yang, W. C., Yalcin, Y., Peck, S., Emons, A. M., van Kammen, A. and Bisseling, T. (1997). Ethylene provides positional information on cortical cell division
but is not involved in Nod factor-induced root hair tip growth in Rhizobium-legume interaction. Development 124, 1781–1787.
Helber, N., Wippel, K., Sauer, N., Schaarschmidt, S., Hause, B. and Requena, N. (2011).
A versatile monosaccharide transporter that operates in the arbuscular mycorrhizal fungus Glomus sp is crucial for the symbiotic relationship with plants. Plant Cell 23, 3812–3823.
Hirsch, A. M. (1992). Developmental biology of legume nodulation. New Phytol 122 , 211–
237.
Hirsch, A. M., Bhuvaneswari, T. V., Torrey, J. G. and Bisseling, T. (1989). Early nodulin
genes are induced in alfalfa root outgrowths elicited by auxin transport inhibitors. Proc
Natl Acad Sci U S A 86, 1244–1248.
Hirsch, S., Kim, J., Munoz, A., Heckmann, A. B., Downie, J. A. and Oldroyd, G. E.
(2009). GRAS proteins form a DNA binding complex to induce gene expression during nodulation signaling in Medicago truncatula. Plant Cell 21, 545–557.
Ho, I. and Trappe, J. M. (1973). Translocation of C from Festuca plants to their
endomycorrhizal fungi. Nat New Biol 244, 30–31.
Horvath, B., Yeun, L. H., Domonkos, A., Halasz, G., Gobbato, E., Ayaydin, F., Miro, K., Hirsch, S., Sun, J., Tadege, M., et al. (2011). Medicago truncatula IPD3 is a member of
the common symbiotic signaling pathway required for rhizobial and mycorrhizal symbioses. Mol Plant Microbe Interact 24, 1345–1358.
Humphreys, C. P., Franks, P. J., Rees, M., Bidartondo, M. I., Leake, J. R. and Beerling, D. J. (2010). Mutualistic mycorrhiza-like symbiosis in the most ancient group of land
plants. Nat Commun 1, 103.
Iizasa, E., Mitsutomi, M. and Nagano, Y. (2010). Direct binding of a plant LysM receptor-
like kinase, LysM RLK1/CERK1, to chitin in vitro. J Biol Chem 285, 2996–3004.
Indrasumunar, A. and Gresshoff, P. M. (2010). Duplicated nod-factor receptor 5 (NFR5)
86
Javot, H., Penmetsa, R. V., Terzaghi, N., Cook, D. R. and Harrison, M. J. (2007a). A
Medicago truncatula phosphate transporter indispensable for the arbuscular mycorrhizal symbiosis. Proc Natl Acad Sci U S A 104, 1720–1725.
Javot, H., Pumplin, N. and Harrison, M. J. (2007b). Phosphate in the arbuscular
mycorrhizal symbiosis: transport properties and regulatory roles. Plant Cell Environ 30, 310–322.
Jin, H. (2009). Arginine bi-directional translocation and breakdown into ornithine along the
arbuscular mycorrhizal mycelium. Science in China. Series C, Life sciences / Chinese
Academy of Sciences 52, 381–9.
Jin, H., Pfeffer, P. E., Douds, D. D., Piotrowski, E., Lammers, P. J. and Shachar-Hill, Y.
(2005). The uptake, metabolism, transport and transfer of nitrogen in an arbuscular mycorrhizal symbiosis. New Phytol 168, 687–696.
Journet, E. P., El-Gachtouli, N., Vernoud, V., de Billy, F., Pichon, M., Dedieu, A., Arnould, C., Morandi, D., Barker, D. G. and Gianinazzi-Pearson, V. (2001).
Medicago truncatula ENOD11: a novel RPRP-encoding early nodulin gene expressed during mycorrhization in arbuscule-containing cells. Mol Plant Microbe Interact 14, 737–748.
Juniper, S. and Abbott, L. (1993). Vesicular-arbuscular mycorrhizas and soil salinity.
Mycorrhiza 4, 45–57.
Kaku, H., Nishizawa, Y., Ishii-Minami, N., Akimoto-Tomiyama, C., Dohmae, N., Takio, K., Minami, E. and Shibuya, N. (2006). Plant cells recognize chitin fragments for
defense signaling through a plasma membrane receptor. Proc Natl Acad Sci U S A 103, 11086–11091.
Kalo, P., Gleason, C., Edwards, A., Marsh, J., Mitra, R. M., Hirsch, S., Jakab, J., Sims, S., Long, S. R., Rogers, J., et al. (2005). Nodulation signaling in legumes requires
NSP2, a member of the GRAS family of transcriptional regulators. Science 308, 1786– 1789.
Kanamori, N., Madsen, L. H., Radutoiu, S., Frantescu, M., Quistgaard, E. M., Miwa, H., Downie, J. A., James, E. K., Felle, H. H., Haaning, L. L., et al. (2006). A nucleoporin
is required for induction of Ca2+ spiking in legume nodule development and essential for rhizobial and fungal symbiosis. Proc Natl Acad Sci U S A 103, 359–364.
Kang, H., Zhu, H., Chu, X., Yang, Z., Yuan, S., Yu, D., Wang, C., Hong, Z. and Zhang, Z. (2011). A novel interaction between CCaMK and a protein containing the Scythe_N
ubiquitin-like domain in Lotus japonicus. Plant Physiol 155, 1312–1324.
Karunakaran, R., Haag, A. F., East, A. K., Ramachandran, V. K., Prell, J., James, E. K., Scocchi, M., Ferguson, G. P. and Poole, P. S. (2010). BacA is essential for bacteroid
development in nodules of galegoid, but not phaseoloid, legumes. J Bacteriol 192, 2920– 2928.
87
Kereszt, A., Mergaert, P., Maroti, G. and Kondorosi, E. (2011a). Innate immunity
effectors and virulence factors in symbiosis. Curr Opin Microbiol 14, 76–81.
Kereszt, A., Mergaert, P. and Kondorosi, E. (2011b). Bacteroid development in legume
nodules: evolution of mutual benefit or of sacrificial victims? Mol Plant Microbe
Interact 24, 1300–1309.
Kevei, Z., Lougnon, G., Mergaert, P., Horvath, G. V., Kereszt, A., Jayaraman, D., Zaman, N., Marcel, F., Regulski, K., Kiss, G. B., et al. (2007). 3-hydroxy-3-
methylglutaryl coenzyme a reductase 1 interacts with NORK and is crucial for nodulation in Medicago truncatula. Plant Cell 19, 3974–3989.
Kiers, E. T., Duhamel, M., Beesetty, Y., Mensah, J. A., Franken, O., Verbruggen, E., Fellbaum, C. R., Kowalchuk, G. A., Hart, M. M., Bago, A., et al. (2011). Reciprocal
rewards stabilize cooperation in the mycorrhizal symbiosis. Science 333, 880–882.
Kosuta, S., Chabaud, M., Lougnon, G., Gough, C., Dénarié, J., Barker, D. G. and Bécard, G. (2003). A diffusible factor from arbuscular mycorrhizal fungi induces
symbiosis-specific MtENOD11 expression in roots of Medicago truncatula. Plant
Physiol 131, 952–962.
Kosuta, S., Hazledine, S., Sun, J., Miwa, H., Morris, R. J., Downie, J. A. and Oldroyd, G. E. (2008). Differential and chaotic calcium signatures in the symbiosis signaling
pathway of legumes. Proc Natl Acad Sci U S A 105, 9823–9828.
Kruger, M., Kruger, C., Walker, C., Stockinger, H. and Schussler, A. (2012).
Phylogenetic reference data for systematics and phylotaxonomy of arbuscular mycorrhizal fungi from phylum to species level. New Phytol 193, 970–984.
Krusell, L., Krause, K., Ott, T., Desbrosses, G., Kramer, U., Sato, S., Nakamura, Y., Tabata, S., James, E. K., Sandal, N., et al. (2005). The sulfate transporter SST1 is
crucial for symbiotic nitrogen fixation in Lotus japonicus root nodules. Plant Cell 17, 1625–1636.
Lefebvre, B., Timmers, T., Mbengue, M., Moreau, S., Hervé, C., Tóth, K., Bittencourt- Silvestre, J., Klaus, D., Deslandes, L., Godiard, L., et al. (2010). A remorin protein
interacts with symbiotic receptors and regulates bacterial infection. Proc Natl Acad Sci U
S A 107, 2343–2348.
Levy, J., Bres, C., Geurts, R., Chalhoub, B., Kulikova, O., Duc, G., Journet, E. P., Ane, J. M., 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.
Lewis, G., Schrire, B., Mackinder, B. and Lock, M. (2005). Legumes of the world. Kew,
Richmond, UK.
Li, F., Hou, B., Chen, L., Yao, Z. and Hong, G. (2008). In vitro observation of the
88 fluorescence resonance energy transfer. Acta Biochim Biophys Sin (Shanghai) 40, 783– 789.
Liao, J., Singh, S., Hossain, M. S., Andersen, S. U., Ross, L., Bonetta, D., Zhou, Y., Sato, S., Tabata, S., Stougaard, J., et al. (2012). Negative regulation of CCaMK is essential
for symbiotic infection. Plant J 72, 572–584.
Lievens, S., Goormachtig, S., Den Herder, J., Capoen, W., Mathis, R., Hedden, P. and Holsters, M. (2005). Gibberellins are involved in nodulation of Sesbania rostrata. Plant
Physiol 139, 1366–1379.
Limpens, E., Franken, C., Smit, P., Willemse, J., Bisseling, T. and Geurts, R. (2003).
LysM domain receptor kinases regulating rhizobial Nod factor-induced infection.