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Transcript Profiling Coupled with Spatial Expression Analyses Reveals Genes Involved in Distinct Developmental Stages of an Arbuscular Mycorrhizal Symbiosis [W]

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Liu, Jinyuan, Blaylock, Laura A., Endre, Gabriella, Cho, Jennifer, Town, Christopher D., VandenBosch, Kathryn A., Harrison, Maria J.·2003·The Plant Cell

DOI 10.1105/tpc.014183

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Abstract

The formation of symbiotic associations with arbuscular mycorrhizal (AM) fungi is a phenomenon common to the majority of vascular flowering plants. Here, we used cDNA arrays to examine transcript profiles in Medicago truncatula roots during the development of an AM symbiosis with Glomus versiforme and during growth under differing phosphorus nutrient regimes. Three percent of the genes examined showed significant changes in transcript levels during the development of the symbiosis. Most genes showing increased transcript levels in mycorrhizal roots showed no changes in response to high phosphorus, suggesting that alterations in transcript levels during symbiosis were a consequence of the AM fungus rather than a secondary effect of improved phosphorus nutrition. Among the mycorrhiza-induced genes, two distinct temporal expression patterns were evident. Members of one group showed an increase in transcripts during the initial period of contact between the symbionts and a subsequent decrease as the symbiosis developed. Defense- and stress-response genes were a significant component of this group. Genes in the second group showed a sustained increase in transcript levels that correlated with the colonization of the root system. The latter group contained a significant proportion of new genes similar to components of signal transduction pathways, suggesting that novel signaling pathways are activated during the development of the symbiosis. Analysis of the spatial expression patterns of two mycorrhiza-induced genes revealed distinct expression patterns consistent with the hypothesis that gene expression in mycorrhizal roots is signaled by both cell-autonomous and cell-nonautonomous signals.

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Molecular Cloning: A Laboratory Manual
Sambrook, J., Fritsch, E., & Maniatis, T. (1989) · UCLA - Biblioteca de Ciencias de la Salud · Cited by 133,589
Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction
Chomczynski, P., & Sacchi, N. (1987) · Analytical Biochemistry · doi:10.1016/0003-2697(87)90021-2 · Cited by 46,426
Cluster analysis and display of genome-wide expression patterns
Eisen, M. B., Spellman, P. T., Brown, P. O., & Botstein, D. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.25.14863 · Cited by 16,184
Genomic sequencing.
Church, G. M., & Gilbert, W. (1984) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.81.7.1991 · Cited by 8,116
A new method which gives an objective measure of colonization of roots by vesicular—arbuscular mycorrhizal fungi
McGONIGLE, T. P., MILLER, M. H., EVANS, D. G., FAIRCHILD, G. L., & SWAN, J. A. (1990) · New Phytologist · doi:10.1111/j.1469-8137.1990.tb00476.x · Cited by 3,878
Mycorrhizal fungal diversity determines plant biodiversity, ecosystem variability and productivity
van der Heijden, M. G. A., Klironomos, J. N., Ursic, M., Moutoglis, P., Streitwolf-Engel, R., Boller, T., Wiemken, A., & Sanders, I. R. (1998) · Nature · doi:10.1038/23932 · Cited by 3,553
[10] Assay of inorganic phosphate, total phosphate and phosphatases
Ames, B. N. (1966) · Methods in Enzymology · doi:10.1016/0076-6879(66)08014-5 · Cited by 3,337
Engineered GFP as a vital reporter in plants
Chiu, W.-L., Niwa, Y., Zeng, W., Hirano, T., Kobayashi, H., & Sheen, J. (1996) · Current Biology · doi:10.1016/s0960-9822(02)00483-9 · Cited by 1,364
A conserved MYB transcription factor involved in phosphate starvation signaling both in vascular plants and in unicellular algae
Rubio, V., Linhares, F., Solano, R., Martín, A. C., Iglesias, J., Leyva, A., & Paz-Ares, J. (2001) · Genes & Development · doi:10.1101/gad.204401 · Cited by 1,343
Mycorrhizal symbiosis
Smith, S. E., Read, D. J., & Harley, J. L. (1997) · Cited by 1,243
Four hundred-million-year-old vesicular arbuscular mycorrhizae.
Remy, W., Taylor, T. N., Hass, H., & Kerp, H. (1994) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.91.25.11841 · Cited by 1,202
Glomalean Fungi from the Ordovician
Redecker, D., Kodner, R., & Graham, L. E. (2000) · Science · doi:10.1126/science.289.5486.1920 · Cited by 1,171
A plant receptor-like kinase required for both bacterial and fungal symbiosis
Stracke, S., Kistner, C., Yoshida, S., Mulder, L., Sato, S., Kaneko, T., Tabata, S., Sandal, N., Stougaard, J., Szczyglowski, K., et al. (2002) · Nature · doi:10.1038/nature00841 · Cited by 951
Gene Expression Profiles during the Initial Phase of Salt Stress in Rice
Kawasaki, S., Borchert, C., Deyholos, M., Wang, H., Brazille, S., Kawai, K., Galbraith, D., & Bohnert, H. J. (2001) · The Plant Cell · doi:10.1105/tpc.13.4.889 · Cited by 934
A receptor kinase gene regulating symbiotic nodule development
Endre, G., Kereszt, A., Kevei, Z., Mihacea, S., Kaló, P., & Kiss, G. B. (2002) · Nature · doi:10.1038/nature00842 · Cited by 832
Self-citation
A Phosphate Transporter from Medicago truncatula Involved in the Acquisition of Phosphate Released by Arbuscular Mycorrhizal Fungi
Harrison, M. J., Dewbre, G. R., & Liu, J. (2002) · The Plant Cell · doi:10.1105/tpc.004861 · Cited by 815
Self-citation
Agrobacterium rhizogenes-Transformed Roots of Medicago truncatula for the Study of Nitrogen-Fixing and Endomycorrhizal Symbiotic Associations
Boisson-Dernier, A., Chabaud, M., Garcia, F., Bécard, G., Rosenberg, C., & Barker, D. G. (2001) · Molecular Plant-Microbe Interactions® · doi:10.1094/mpmi.2001.14.6.695 · Cited by 751
The origin of land plants: A matter of mycotrophism
Pirozynski, K. A., & Malloch, D. W. (1975) · Biosystems · doi:10.1016/0303-2647(75)90023-4 · Cited by 698
Rice phosphate transporters include an evolutionarily divergent gene specifically activated in arbuscular mycorrhizal symbiosis
Paszkowski, U., Kroken, S., Roux, C., & Briggs, S. P. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.202474599 · Cited by 688
Crop production in artificial culture solutions and in soils with special reference to factors influencing yields and absorption of inorganic nutrients.
Arnon, D. I., & Hoagland, D. R. (1940) · Soil Science · Cited by 651
Genomic Analysis of a Nutrient Response in Arabidopsis Reveals Diverse Expression Patterns and Novel Metabolic and Potential Regulatory Genes Induced by Nitrate
Wang, R., Guegler, K., LaBrie, S. T., & Crawford, N. M. (2000) · The Plant Cell · doi:10.1105/tpc.12.8.1491 · Cited by 578
A plasma membrane-bound putative endo-1,4-beta -D-glucanase is required for normal wall assembly and cell elongation in Arabidopsis
Nicol, F. (1998) · The EMBO Journal · doi:10.1093/emboj/17.19.5563 · Cited by 574
Rapamycin-modulated transcription defines the subset of nutrient-sensitive signaling pathways directly controlled by the Tor proteins
Hardwick, J. S., Kuruvilla, F. G., Tong, J. K., Shamji, A. F., & Schreiber, S. L. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.26.14866 · Cited by 522
A phosphate transporter expressed in arbuscule-containing cells in potato
Rausch, C., Daram, P., Brunner, S., Jansa, J., Laloi, M., Leggewie, G., Amrhein, N., & Bucher, M. (2001) · Nature · doi:10.1038/35106601 · Cited by 479
Plant Cell Responses to Arbuscular Mycorrhizal Fungi: Getting to the Roots of the Symbiosis.
Gianinazzi-Pearson, V. (1996) · The Plant Cell · doi:10.1105/tpc.8.10.1871 · Cited by 440
The NAF domain defines a novel protein-protein interaction module conserved in Ca2+-regulated kinases
Albrecht, V. (2001) · The EMBO Journal · doi:10.1093/emboj/20.5.1051 · Cited by 397
A Diffusible Factor from Arbuscular Mycorrhizal Fungi Induces Symbiosis-Specific MtENOD11 Expression in Roots of Medicago truncatula
Kosuta, S., Chabaud, M., Lougnon, G., Gough, C., Dénarié, J., Barker, D. G., & Bécard, G. (2003) · Plant Physiology · doi:10.1104/pp.011882 · Cited by 347
Medicago truncatula ENOD11: A Novel RPRP-Encoding Early Nodulin Gene Expressed During Mycorrhization in Arbuscule-Containing Cells
Journet, E.-P., El-Gachtouli, N., Vernoud, V., de Billy, F., Pichon, M., Dedieu, A., Arnould, C., Morandi, D., Barker, D. G., & Gianinazzi-Pearson, V. (2001) · Molecular Plant-Microbe Interactions® · doi:10.1094/mpmi.2001.14.6.737 · Cited by 299
Rapid Induction of Regulatory and Transporter Genes in Response to Phosphorus, Potassium, and Iron Deficiencies in Tomato Roots. Evidence for Cross Talk and Root/Rhizosphere-Mediated Signals
Wang, Y.-H., Garvin, D. F., & Kochian, L. V. (2002) · Plant Physiology · doi:10.1104/pp.008854 · Cited by 290
Isoflavonoid Accumulation and Expression of Defense Gene Transcripts During the Establishment of Vesicular-Arbuscular Mycorrhizal Associations in Roots of Medicago truncatula
Harrison, M. J. (1993) · Molecular Plant-Microbe Interactions · doi:10.1094/mpmi-6-643 · Cited by 284
Self-citation
Cloning and Characterization of Two Phosphate Transporters from Medicago truncatula Roots: Regulation in Response to Phosphate and to Colonization by Arbuscular Mycorrhizal (AM) Fungi
Liu, H., Trieu, A. T., Blaylock, L. A., & Harrison, M. J. (1998) · Molecular Plant-Microbe Interactions® · doi:10.1094/mpmi.1998.11.1.14 · Cited by 281
Self-citation
Tansley Review No. 82. Strategies of arbuscular mycorrhizal fungi when infecting host plants
BONFANTE, P., & PEROTTO, S. (1995) · New Phytologist · doi:10.1111/j.1469-8137.1995.tb01810.x · Cited by 269
KORRIGAN, an Arabidopsis Endo-1,4-β-Glucanase, Localizes to the Cell Plate by Polarized Targeting and Is Essential for Cytokinesis
Zuo, J., Niu, Q.-W., Nishizawa, N., Wu, Y., Kost, B., & Chua, N.-H. (2000) · The Plant Cell · doi:10.1105/tpc.12.7.1137 · Cited by 267
Psr1, a nuclear localized protein that regulates phosphorus metabolism in Chlamydomonas
Wykoff, D. D., Grossman, A. R., Weeks, D. P., Usuda, H., & Shimogawara, K. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.26.15336 · Cited by 258
Genome-Wide Identification of Nodule-Specific Transcripts in the Model Legume Medicago truncatula
Fedorova, M., van de Mortel, J., Matsumoto, P. A., Cho, J., Town, C. D., VandenBosch, K. A., Gantt, J. S., & Vance, C. P. (2002) · Plant Physiology · doi:10.1104/pp.006833 · Cited by 245
Self-citation
The Roles of Auxins and Cytokinins in Mycorrhizal Symbioses
Barker, S. J., & Tagu, D. (2000) · Journal of Plant Growth Regulation · doi:10.1007/s003440000021 · Cited by 243
Induction of Jasmonate Biosynthesis in Arbuscular Mycorrhizal Barley Roots,
Hause, B., Maier, W., Miersch, O., Kramell, R., & Strack, D. (2002) · Plant Physiology · doi:10.1104/pp.006007 · Cited by 239
Cloning of the SNG1 Gene of Arabidopsis Reveals a Role for a Serine Carboxypeptidase-like Protein as an Acyltransferase in Secondary Metabolism
Lehfeldt, C., Shirley, A. M., Meyer, K., Ruegger, M. O., Cusumano, J. C., Viitanen, P. V., Strack, D., & Chapple, C. (2000) · The Plant Cell · doi:10.1105/tpc.12.8.1295 · Cited by 236
BRS1, a serine carboxypeptidase, regulates BRI1 signaling in Arabidopsis thaliana
Li, J., Lease, K. A., Tax, F. E., & Walker, J. C. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.091065998 · Cited by 229
Expression of early nodulin genes in alfalfa mycorrhizae indicates that signal transduction pathways used in forming arbuscular mycorrhizae and Rhizobium-induced nodules may be conserved
van Rhijn, P., Fang, Y., Galili, S., Shaul, O., Atzmon, N., Wininger, S., Eshed, Y., Lum, M., Li, Y., To, V., et al. (1997) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.94.10.5467 · Cited by 214
Rhizobial Nodulation Factors Stimulate Mycorrhizal Colonization of Nodulating and Nonnodulating Soybeans
Xie, Z. P., Staehelin, C., Vierheilig, H., Wiemken, A., Jabbouri, S., Broughton, W. J., Vogeli-Lange, R., & Boller, T. (1995) · Plant Physiology · doi:10.1104/pp.108.4.1519 · Cited by 209
Zinc Deficiency Up-Regulates Expression of High-Affinity Phosphate Transporter Genes in Both Phosphate-Sufficient and -Deficient Barley Roots
Huang, C., Barker, S. J., Langridge, P., Smith, F. W., & Graham, R. D. (2000) · Plant Physiology · doi:10.1104/pp.124.1.415 · Cited by 207
Differential Expression of Eight Chitinase Genes in Medicago truncatula Roots During Mycorrhiza Formation, Nodulation, and Pathogen Infection
Salzer, P., Bonanomi, A., Beyer, K., Vögeli-Lange, R., Aeschbacher, R. A., Lange, J., Wiemken, A., Kim, D., Cook, D. R., & Boller, T. (2000) · Molecular Plant-Microbe Interactions® · doi:10.1094/mpmi.2000.13.7.763 · Cited by 202
Exploring root symbiotic programs in the model legume Medicago truncatula using EST analysis
Journet, E.-P. (2002) · Nucleic Acids Research · doi:10.1093/nar/gkf685 · Cited by 193
Endo-β-1,4-Glucanase Expression in Compatible Plant–Nematode Interactions
Mitchum, M. G., Wang, X., & Davis, E. (2001) · The Plant Cell · doi:10.1105/tpc.010219 · Cited by 157
Dynamics of arbuscule development and degeneration in onion, bean, and tomato with reference to vesicular–arbuscular mycorrhizae in grasses
Alexander, T., Toth, R., Meier, R., et al. (1989) · Canadian Journal of Botany · doi:10.1139/b89-320 · Cited by 155
Transcriptional Changes in Response to Arbuscular Mycorrhiza Development in the Model Plant Medicago truncatula
Wulf, A., Manthey, K., Doll, J., Perlick, A. M., Linke, B., Bekel, T., Meyer, F., Franken, P., Küster, H., & Krajinski, F. (2003) · Molecular Plant-Microbe Interactions · doi:10.1094/mpmi.2003.16.4.306 · Cited by 154
A membrane-anchored E-type endo-1,4-β-glucanase is localized on Golgi and plasma membranes of higher plants
Brummell, D. A., Catalá, C., Lashbrook, C. C., et al. (1997) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.94.9.4794 · Cited by 140
Suppression of Endochitinase,β-1,3-Endoglucanase, and Chalcone Isomerase Expression in Bean Vesicular-Arbuscular Mycorrhizal Roots Under Different Soil Phosphate Conditions
Lambais, M. R. (1993) · Molecular Plant-Microbe Interactions · doi:10.1094/mpmi-6-075 · Cited by 139
A novel gene whose expression in Medicago truncatula roots is suppressed in response to colonization by vesicular-arbuscular mycorrhizal (VAM) fungi and to phosphate nutrition
Burleigh, S., & Harrison, M. (1997) · Plant Molecular Biology · doi:10.1023/a:1005841119665 · Cited by 129
Self-citation
An acyltransferase catalyzing the formation of diacylglucose is a serine carboxypeptidase-like protein
Li, A. X., & Steffens, J. C. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.110154197 · Cited by 108
Identification of a novel genetically controlled step in mycorrhizal colonization: plant resistance to infection by fungal spores but not extra‐radical hyphae
David‐Schwartz, R., Badani, H., Wininger, S., et al. (2001) · The Plant Journal · doi:10.1046/j.1365-313x.2001.01113.x · Cited by 106
Novel Genes Induced During an Arbuscular Mycorrhizal (AM) Symbiosis Formed Between Medicago truncatula and Glomus versiforme
van Buuren, M. L., Maldonado‐Mendoza, I. E., Trieu, A. T., Blaylock, L. A., & Harrison, M. (1999) · Molecular Plant-Microbe Interactions · doi:10.1094/mpmi.1999.12.3.171 · Cited by 104
Self-citation
Actin versus tubulin configuration in arbuscule‐containing cells from mycorrhizal tobacco roots
Genre, A., & Bonfante, P. (1998) · New Phytologist · doi:10.1046/j.1469-8137.1998.00314.x · Cited by 95
Microtubule organization in root cells ofMedicago truncatula during development of an arbuscular mycorrhizal symbiosis withGlomus versiforme
Blancaflor, E. B., Zhao, L., & Harrison, M. (2001) · PROTOPLASMA · doi:10.1007/bf01283396 · Cited by 83
Self-citation
Suppression of defence responses in mycorrhizal alfalfa and tobacco roots
Kapulnik, Y., Volpin, H., Itzhaki, H., GANON, D., Galili, S., David, R. D., Shaul, O., Elad, Y., Chet, I., & Okon, Y. (1996) · New Phytologist · doi:10.1111/j.1469-8137.1996.tb04341.x · Cited by 83
Transcriptional activation of a maize α‐tubulin gene in mycorrhizal maize and transgenic tobacco plants
Bonfante, P., Bergero, R., Uribe, X., Romera, C., Rigau, J., & Puigdomènech, P. (1996) · The Plant Journal · doi:10.1046/j.1365-313x.1996.9050737.x · Cited by 81
Colonization of Pea Roots by the Mycorrhizal FungusGlomus versiformeand byRhizobiumBacteria: Immunological Comparison Using Monoclonal Antibodies as Probes for Plant Cell Surface Components
Perotto, S. (1994) · Molecular Plant-Microbe Interactions · doi:10.1094/mpmi-7-0091 · Cited by 70
A mycorrhizal fungus changes microtubule orientation in tobacco root cells
Genre, A., & Bonfante, P. (1997) · PROTOPLASMA · doi:10.1007/bf02539803 · Cited by 69
The Involvement of a Cysteine Proteinase in the Nodule Development in Chinese Milk Vetch Infected with Mesorhizobium huakuii subsp. rengei
Naito, Y., Fujie, M., Usami, S., Murooka, Y., & Yamada, T. (2000) · PLANT PHYSIOLOGY · doi:10.1104/pp.124.3.1087 · Cited by 66
Response of Symbiotic Endomycorrhizal Fungi to Estrogens and Antiestrogens
Poulin, M.-J., Simard, J., Catford, J.-G., Librie, F., & Piché, Y. (1997) · Molecular Plant-Microbe Interactions · doi:10.1094/mpmi.1997.10.4.481 · Cited by 55
Primary structure of carboxypeptidase III from malted barley
Sørensen, S. B., Svendsen, I., & Breddam, K. (1989) · Carlsberg Research Communications · doi:10.1007/bf02904473 · Cited by 51
Primary structure of carboxypeptidase II from malted barley
Sørensen, S. B., Svendsen, I., & Breddam, K. (1987) · Carlsberg Research Communications · doi:10.1007/bf02907171 · Cited by 36

Phylogenetic distribution and evolution of mycorrhizas in land plants
Wang, B., & Qiu, Y.-L. (2006) · Mycorrhiza · doi:10.1007/s00572-005-0033-6 · Cited by 1,920
Unraveling mycorrhiza-induced resistance
Pozo, M. J., & Azcón-Aguilar, C. (2007) · Current Opinion in Plant Biology · doi:10.1016/j.pbi.2007.05.004 · Cited by 1,157
Mycorrhiza-Induced Resistance and Priming of Plant Defenses
Jung, S. C., Martinez-Medina, A., Lopez-Raez, J. A., & Pozo, M. J. (2012) · Journal of Chemical Ecology · doi:10.1007/s10886-012-0134-6 · Cited by 1,019
Invasive Plant Suppresses the Growth of Native Tree Seedlings by Disrupting Belowground Mutualisms
Stinson, K. A., Campbell, S. A., Powell, J. R., Wolfe, B. E., Callaway, R. M., Thelen, G. C., Hallett, S. G., Prati, D., & Klironomos, J. N. (2006) · PLoS Biology · doi:10.1371/journal.pbio.0040140 · Cited by 826
SIGNALING IN THE ARBUSCULAR MYCORRHIZAL SYMBIOSIS
Harrison, M. J. (2005) · Annual Review of Microbiology · doi:10.1146/annurev.micro.58.030603.123749 · Cited by 785
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Authors: Liu, J., Blaylock, L. A., Endre, G., Cho, J., Town, C. D., VandenBosch, K. A., & Harrison, M. J.
Venue: The Plant Cell
Publisher: Oxford University Press (OUP)
Published: 2003-09-01
Volume: 15
Issue: 9
Pages: 2106-2123
ISSN: 1040-4651 (ISSN-L)
1532-298X
DOI: 10.1105/tpc.014183
OpenAlex: W2108372550
Cited by: 337
References: 63
FWCI: 24.85
Type: journal article
Language: en
Open access: bronze

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Transcript Profiling Coupled with Spatial Expression Analyses Reveals Genes Involved in Distinct Developmental Stages of an Arbuscular Mycorrhizal Symbiosis [W]

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