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Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
REVIEW

Transcriptional snapshots provide insights into the molecular basis of arbuscular mycorrhiza in the model legume Medicago truncatula

Natalija Hohnjec A B , Kolja Henckel C , Thomas Bekel C , Jerome Gouzy D , Michael Dondrup B C , Alexander Goesmann C and Helge Küster A B E
+ Author Affiliations
- Author Affiliations

A Institute for Genome Research, Center for Biotechnology (CeBiTec), Bielefeld University, D-33594 Bielefeld, Germany.

B International Graduate School in Bioinformatics and Genome Research, Center for Biotechnology (CeBiTec), Bielefeld University, D-33594 Bielefeld, Germany.

C Bioinformatics Resource Facility, Center for Biotechnology (CeBiTec), Bielefeld University, D-33594 Bielefeld, Germany.

D Laboratoire des Interactions Plantes Micro-organismes LIPM, Chemin de Borde-Rouge–Auzeville, BP 52627, 31326 Castanet Tolosan, Cedex, France.

E Corresponding author. Email: Helge.Kuester@Genetik.Uni-Bielefeld.DE

F This paper originates from a presentation at the Third International Conference on Legume Genomics and Genetics, Brisbane, Queensland, Australia, April 2006.

Functional Plant Biology 33(8) 737-748 https://doi.org/10.1071/FP06079
Submitted: 5 April 2006  Accepted: 15 June 2006   Published: 2 August 2006

Abstract

The arbuscular mycorrhizal (AM) association between terrestrial plants and soil fungi of the phylum Glomeromycota is the most widespread beneficial plant–microbe interaction on earth. In the course of the symbiosis, fungal hyphae colonise plant roots and supply limiting nutrients, in particular phosphorus, in exchange for carbon compounds. Owing to the obligate biotrophy of mycorrhizal fungi and the lack of genetic systems to study them, targeted molecular studies on AM symbioses proved to be difficult. With the emergence of plant genomics and the selection of suitable models, an application of untargeted expression profiling experiments became possible. In the model legume Medicago truncatula, high-throughput expressed sequence tag (EST)-sequencing in conjunction with in silico and experimental transcriptome profiling provided transcriptional snapshots that together defined the global genetic program activated during AM. Owing to an asynchronous development of the symbiosis, several hundred genes found to be activated during the symbiosis cannot be easily correlated with symbiotic structures, but the expression of selected genes has been extended to the cellular level to correlate gene expression with specific stages of AM development. These approaches identified marker genes for the AM symbiosis and provided the first insights into the molecular basis of gene expression regulation during AM.

Keywords: arbuscule-specific genes, EST-sequencing, expression databases, Glomus spp., in silico transcriptome profiling, microarray-based transcriptome profiling, TIGR M. truncatula Gene Index.


Acknowledgments

This work was supported by the Deutsche Forschungsgemeinschaft SPP 1084 ‘Mykorrhiza’ as well as by the European Union projects MEDICAGO (QLG-CT2000–00676) and GRAIN LEGUMES (FOOD-CT-2004–506223). HK, MD and NH acknowledge financial support by the International Graduate School in Bioinformatics and Genome Research. The work of AG and TB was funded by the Bundesministerium für Bildung und Forschung (BMBF 0313105).


References


Alba R, Zhangjun F, Payton P, Liu Y, Moore SL , et al. (2004) ESTs, cDNA microarrays, and gene expression profiling: tools for dissecting plant physiology and development. The Plant Journal 39, 697–714.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Albrecht C, Geurts R, Lapeyrie F, Bisseling T (1998) Endomycorrhizae and rhizobial Nod factors both require SYM8 to induce the expression of the early nodulin genes PsENOD5 and PsENOD12A. The Plant Journal 15, 605–614.
Crossref | GoogleScholarGoogle Scholar | open url image1

Allison DB, Cui X, Page GP, Sabripour M (2006) Microarray data analysis: from disarray to consolidation and consensus. Nature Reviews. Genetics 7, 55–65.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Bago B, Pfeffer PE, Shachar-Hill Y (2000) Carbon metabolism and transport in arbuscular mycorrhizas. Plant Physiology 124, 949–958.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Barker DG, Bianchi S, Blondon F, Dattée Y, Duc G , et al. (1990) Medicago truncatula, a model plant for studying the molecular genetics of the Rhizobium–legume symbiosis. Plant Molecular Biology Reporter 8, 40–49. open url image1

Boisson-Dernier A, Andriankaja A, Chabaud M, Niebel A, Journet E-P, Barker DG, de Carvalho-Niebel F (2005) MtEnod11 gene activation during rhizobial infection and mycorrhizal arbuscule development requires a common AT-rich-containing regulatory sequence. Molecular Plant–Microbe Interactions 18, 1269–1276.
PubMed |
open url image1

Bonfante P, Perotto S (1995) Strategies of arbuscular mycorrhizal fungi when infecting host plants. New Phytologist 130, 3–21.
Crossref | GoogleScholarGoogle Scholar | open url image1

Brechenmacher L, Weidmann S, van Tuinen D, Chatagnier O, Gianinazzi S, Franken P, Gianinazzi-Pearson V (2004) Expression profiling of up-regulated plant and fungal genes in early and late stages of Medicago truncatulaGlomus mosseae interactions. Mycorrhiza 14, 253–262.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Brewin NJ (1991) Development of the legume root nodule. Annual Review of Cell Biology 7, 191–226.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Chabaud M, Venard C, Defaux-Petras A, Bécard G, Barker DG (2002) Targeted inoculation of Medicago truncatula in vitro root cultures reveals MtENOD11 expression during early stages of infection by arbuscular mycorrhizal fungi. New Phytologist 156, 265–273.
Crossref | GoogleScholarGoogle Scholar | open url image1

Colebatch G, Kloska S, Trevaskis B, Freund S, Altmann T, Udvardi MK (2002) Novel aspects of symbiotic nitrogen fixation uncovered by transcript profiling with cDNA arrays. Molecular Plant–Microbe Interactions 15, 411–420.
PubMed |
open url image1

Colebatch G, Desbrosses G, Ott T, Krusell L, Montanari O, Kloska S, Kopka J, Udvardi MK (2004) Global changes in transcription orchestrate metabolic differentiation during symbiotic nitrogen fixation in Lotus japonicus. The Plant Journal 39, 487–512.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Cullimore J, Dénarié J (2003) How legumes select their sweet talking symbionts. Science 302, 575–578.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Czechowski T, Bari RP, Stitt M, Scheible WR, Udvardi MK (2004) Real-time RT–PCR profiling of over 1400 Arabidopsis transcription factors: unprecedented sensitivity reveals novel root- and shoot-specific genes. The Plant Journal 38, 366–379.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Diatchenko L, Lau YF, Campbell AP, Chenchik A, Moqadam F , et al. (1996) Suppression subtractive hybridization: a method for generating differentially regulated or tissue-specific cDNA probes and libraries. Proceedings of the National Academy of Sciences USA 93, 6025–6030.
Crossref | GoogleScholarGoogle Scholar | open url image1

Doll J, Hause B, Demchenko K, Pawlowski K, Krajinski F (2003) A member of the germin-like protein family is a highly conserved mycorrhiza-specific induced gene. Plant & Cell Physiology 44, 1208–1214.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Dondrup M, Goesmann A, Bartels D, Kalinowski J, Krause L, Linke B, Rupp O, Szyrba A, Pühler A, Meyer F (2003) EMMA: a platform for consistent storage and efficient analysis of microarray data. Journal of Biotechnology 106, 135–146.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

El Yahyaoui F, Küster H, Ben Amor B, Hohnjec N, Pühler A , et al. (2004) Expression profiling in Medicago truncatula identifies more than 750 genes differentially expressed during nodulation, including many potential regulators of the symbiotic program. Plant Physiology 136, 3159–3176.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Fedorova M, van de Mortel J, Matsumoto PA, Cho J, Town CD, VandenBosch KA, Gantt JS, Vance CP (2002) Genome-wide identification of nodule-specific transcripts in the model legume Medicago truncatula. Plant Physiology 130, 519–537.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Fehlberg V, Vieweg MF, Dohmann EMN, Hohnjec N, Pühler A, Perlick AM, Küster H (2005) The promoter of the leghaemoglobin gene VfLb29: functional analysis and identification of modules necessary for its activation in the infected cells of root nodules and in the arbuscule-containing cells of mycorrhizal roots. Journal of Experimental Botany 56, 799–806.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Ferrol N, Pozo MJ, Antelo M, Azcon-Aguilar C (2002) Arbuscular mycorrhizal symbiosis regulates plasma membrane H+-ATPase gene expression in tomato plants. Journal of Experimental Botany 53, 1683–1687.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Franken P, Requena N (2001) Analysis of gene expression in arbuscular mycorrhiza: new approaches and challenges. New Phytologist 150, 431–439.
Crossref |
open url image1

Frenzel A, Manthey K, Perlick AM, Meyer F, Pühler A, Krajinski F, Küster H (2005) Combined transcriptome profiling reveals a novel family of arbuscular mycorrhizal-specific Medicago truncatula lectin genes. Molecular Plant–Microbe Interactions 18, 771–782.
PubMed |
open url image1

Frühling M, Roussel H, Gianinazzi-Pearson V, Pühler A, Perlick AM (1997) The Vicia faba leghemoglobin gene VfLb29 is induced in root nodules and in roots colonized by the arbuscular mycorrhizal fungus Glomus fasciculatum. Molecular Plant–Microbe Interactions 10, 124–131.
PubMed |
open url image1

Genre A, Chabaud M, Timmers T, Bonfante P, Barker DG (2005) Arbuscular mycorrhizal fungi elicit a novel intracellular apparatus in Medicago truncatula root epidermal cells before infection. The Plant Cell 17, 3489–3499.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Geurts R, Fedorova E, Bisseling T (2005) Nod factor signaling genes and their function in the early stages of Rhizobium infection. Current Opinion in Plant Biology 8, 346–352.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Gianinazzi-Pearson V (1996) Plant cell responses to arbuscular mycorrhizal fungi: getting to the roots of the symbiosis. The Plant Cell 8, 1871–1883.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Gianinazzi-Pearson V, Dénarié J (1997) Red carpet genetic programmes for root endosymbioses. Trends in Plant Science 2, 371–372.
Crossref | GoogleScholarGoogle Scholar | open url image1

Gianinazzi-Pearson V, Brechenmacher L (2004) Functional genomics of arbuscular mycorrhiza: decoding the symbiotic cell programme. Canadian Journal of Botany 82, 1228–1234.
Crossref | GoogleScholarGoogle Scholar | open url image1

Gianinazzi-Pearson V, Arnould C, Oufattole M, Arango M, Gianinazzi S (2000) Differential activation of H+-ATPase genes by an arbuscular mycorrhizal fungus in root cells of transgenic tobacco. Planta 211, 609–613.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Graham JH, Miller M (2005) Mycorrhizas: gene to function. Plant and Soil 274, 79–100.
Crossref | GoogleScholarGoogle Scholar | open url image1

Grunwald U, Nyamsuren O, Tamasloukht M, Lapopin L, Becker A, Mann P, Gianinazzi-Pearson V, Krajinski F, Franken P (2004) Identification of mycorrhiza-regulated genes with arbuscule development-related expression profile. Plant Molecular Biology 55, 553–566.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Handberg K, Stougaard J (1992) Lotus japonicus, an autogamous, diploid legume species for classical and molecular genetics. The Plant Journal 2, 487–496.
Crossref | GoogleScholarGoogle Scholar | open url image1

Harrison MJ (1996) A sugar transporter from Medicago truncatula: altered expression pattern in roots during vesicular-arbuscular (VA) mycorrhizal associations. The Plant Journal 9, 491–503.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Harrison MJ (1997) The arbuscular mycorrhizal symbiosis: an underground association. Trends in Plant Science 2, 54–60.
Crossref | GoogleScholarGoogle Scholar | open url image1

Harrison MJ (1999) Molecular and cellular aspects of the arbuscular mycorrhizal symbiosis. Annual Review of Plant Physiology and Plant Molecular Biology 50, 361–389.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Harrison MJ (2005) Signaling in the arbuscular mycorrhizal symbiosis. Annual Review of Microbiology 59, 19–42.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Harrison MJ, Dewbre GR, Liu J (2002) A phosphate transporter from Medicago truncatula involved in the acquisition of phosphate released by arbuscular mycorrhizal fungi. The Plant Cell 14, 2413–2429.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Hijri M, Sanders IR (2004) The arbuscular mycorrhizal fungus Glomus intraradices is haploid and has a small genome size in the lower limit of eukaryotes. Fungal Genetics and Biology 41, 253–261.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Hohnjec N, Vieweg MF, Pühler A, Becker A, Küster H (2005) Overlaps in the transcriptional profiles of Medicago truncatula roots inoculated with two different Glomus fungi provide insights into the genetic program activated during arbuscular mycorrhiza. Plant Physiology 137, 1283–1301.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Hraber PT, Weller JW (2001) On the species of origin: diagnosing the source of symbiotic transcripts. Genome Biology 2, 0037.1–0037.14.
Crossref | GoogleScholarGoogle Scholar | open url image1

Isayenkov S, Mrosk C, Stenzel I, Strack D, Hause B (2005) Suppression of allene oxide cyclase in hairy roots of M. truncatula reduces jasmonate levels and the degree of mycorrhization with Glomus intraradices. Plant Physiology 139, 1401–1410.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Ivashuta S, Liu J, Liu J, Lohar DP, Haridas S, Bucciarelli B, VandenBosch KA, Vance CP, Harrison MJ, Gantt JS (2005) RNA interference identifies a calcium-dependent protein kinase involved in Medicago truncatula root development. The Plant Cell 17, 2911–2921.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Journet EP, El-Gachtouli N, Vernoud V, de Billy F, Pichon M, Dedieu A, Arnould C, Morandi D, Barker DG, Gianinazzi-Pearson V (2001) Medicago truncatula ENOD11: a novel RPRP-encoding early nodulin gene expressed during mycorrhization in arbuscule-containing cells. Molecular Plant–Microbe Interactions 14, 737–748.
PubMed |
open url image1

Journet EP, van Tuinen D, Gouzy J, Crespeau H, Carreau V , et al. (2002) Exploring root symbiotic programs in the model legume Medicago truncatula using EST analysis. Nucleic Acids Research 30, 5579–5592.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Kehr J (2003) Single cell technology. Current Opinion in Plant Biology 6, 617–621.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Kerk NM, Ceserani T, Tausta SL, Sussex IM, Nelson TM (2003) Laser capture microdissection of cells from plant tissues. Plant Physiology 132, 27–35.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Kistner C, Parniske M (2002) Evolution of signal transduction intracellular symbiosis. Trends in Plant Science 7, 511–518.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Kistner C, Winzer T, Pitzschke A, Mulder L, Sato S , et al. (2005) Seven Lotus japonicus genes required for transcriptional reprogramming of the root during fungal and bacterial symbiosis. The Plant Cell 17, 2217–2229.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Kosuta S, Chabaud M, Lougnon G, Gough C, Dénarié J, Barker DG, Bécard G (2003) A diffusible factor from arbuscular mycorrhizal fungi induces symbiosis-specific MtENOD11 expression in roots of Medicago truncatula. Plant Physiology 131, 952–962.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Kouchi H, Shimomura K, Hata S, Hirota A, Wu G-J , et al. (2004) Large-scale analysis of gene expression profiles during early stages of root nodule formation in a model legume, Lotus japonicus. DNA Research 11, 263–274.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Krajinski F, Biela A, Schubert D, Gianinazzi-Pearson V, Kaldenhoff R, Franken P (2000) Arbuscular mycorrhiza development regulates the mRNA abundance of Mtaqp1 encoding a mercury-insensitive aquaporin of Medicago truncatula. Planta 211, 85–90.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Krajinski F, Hause B, Gianinazzi-Pearson V, Franken P (2002) Mtha1, a plasma membrane H+-ATPase gene from Medicago truncatula, shows arbuscule-induced expression. Plant Biology 4, 754–761.
Crossref | GoogleScholarGoogle Scholar | open url image1

Küster H, Hohnjec N, Krajinski F, El Yahyaoui F, Manthey K , et al. (2004) Construction and validation of cDNA-based Mt6k-RIT macro- and microarrays to explore root endosymbioses in the model legume Medicago truncatula. Journal of Biotechnology 108, 95–113.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Lammers P, Tuskan GA, DiFazio SP, Podila GK, Martin F (2004) Mycorrhizal symbionts of Populus to be sequenced by the United States Department of Energy’s Joint Genome Institute. Mycorrhiza 14, 63–64.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Limpens E, Bisseling T (2003) Signaling in symbiosis. Current Opinion in Plant Biology 6, 343–350.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Liu J, Blaylock LA, Endre G, Cho J, Town CD, VandenBosch KA, Harrison MJ (2003) Transcript profiling coupled with spatial expression analyses reveals genes involved in distinct developmental stages of an arbuscular mycorrhizal symbiosis. The Plant Cell 15, 2106–2123.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Lohar DP, Sharopova N, Endre S, Peñuela S, Samac D, Town C, Silverstein KAT, VandenBosch KA (2006) Transcript analysis of early nodulation events in Medicago truncatula. Plant Physiology 140, 221–234.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Manthey K, Krajinski F, Hohnjec N, Firnhaber C, Pühler A, Perlick AM, Küster H (2004) Transcriptome profiling in root nodules and arbuscular mycorrhiza identifies a collection of novel genes induced during Medicago truncatula root endosymbioses. Molecular Plant–Microbe Interactions 17, 1063–1077.
PubMed |
open url image1

Martin F, Tuskan GA, DiFazio SP, Lammers P, Newcombe G, Podila GK (2004) Symbiotic sequencing of the Populus mesocosm. New Phytologist 161, 330–335.
Crossref | GoogleScholarGoogle Scholar | open url image1

Meyer F, Goesmann A, McHardy AC, Bartels D, Bekel T , et al. (2003) GenDB: an open source genome annotation system for prokaryote genomes. Nucleic Acids Research 31, 2187–2195.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Parniske M (2000) Intracellular accommodation of microbes by plants: a common developmental program for symbiosis and disease? Current Opinion in Plant Biology 3, 320–328.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Provorov NA, Borisov AY, Tikhonovich IA (2002) Developmental genetics and evolution of symbiotic structures in nitrogen-fixing nodules and arbuscular mycorrhiza. Journal of Theoretical Biology 214, 215–232.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Quackenbush J, Cho J, Lee D, Liang F, Holt I, Karamycheva S, Parvici B, Pertea G, Sultana R, White J (2001) The TIGR Gene Indices: analysis of gene transcript sequences in highly sampled eukaryotic species. Nucleic Acids Research 29, 159–164.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Rausch C, Daram P, Brunner S, Jansa J, Laloi M, Leggewie G, Amrhein N, Bucher M (2001) A phosphate transporter expressed in arbuscule-containing cells of potato. Nature 414, 462–466.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Requena N, Breuninger M, Franken P, Ocon A (2003) Symbiotic status, phosphate, and sucrose regulate the expression of two plasma membrane H+-ATPase genes from the mycorrhizal fungus Glomus mosseae. Plant Physiology 132, 1540–1549.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Rosewarne GM, Barker SJ, Smith SE (1997) Production of near-synchronous fungal colonization in tomato for developmental and molecular analyses of mycorrhiza. Mycological Research 101, 966–970.
Crossref | GoogleScholarGoogle Scholar | open url image1

Salzer P, Bonanomi A, Beyer K, Vogeli-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. Molecular Plant–Microbe Interactions 13, 763–777.
PubMed |
open url image1

Sato S, Tabata S (2006) Lotus japonicus as a platform for legume research. Current Opinion in Plant Biology 9, 128–132.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Schiex T, Gouzy J, Moisan A, de Oliveira Y (2003) FrameD: a flexible program for quality check and gene prediction in prokaryotic genomes and noisy matured eukaryotic sequences. Nucleic Acids Research 31, 3738–3741.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Schüssler A, Schwarzott D, Walker C (2001) A new fungal phylum, the Glomeromycota: phylogeny and evolution. Mycological Research 105, 1413–1421. open url image1

Shachar-Hill Y, Pfeffer PE, Douds D, Osman SF, Doner LW, Ratcliffe RG (1995) Partitioning of intermediate carbon metabolism in VAM colonized leek. Plant Physiology 108, 7–15.
PubMed |
open url image1

Smith SE, Dickson S, Smith FA (2001) Nutrient transfer in arbuscular mycorrhizas: how are fungal and plant processes integrated? Australian Journal of Plant Physiology 28, 683–694. open url image1

Smith SE , Read DJ (1997) ‘Mycorrhizal symbiosis.’ (Academic Press: London)

Stacey G, Libault M, Brechenmacher L, Wan J, May GD (2006) Genetics and functional genomics of legume nodulation. Current Opinion in Plant Biology 9, 110–121.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Stekel DJ, Git Y, Falciani F (2000) The comparison of gene expression from multiple cDNA libraries. Genome Research 10, 2055–2061.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Stougaard J, Sandal N, Gron A, Kuhle A, Marcker K (1987) 5′ analysis of the soybean leghaemoglobin lbc3 gene: regulatory elements required for promoter activity and organ specificity. EMBO Journal 6, 3565–3569.
PubMed |
open url image1

Tadege M, Ratet P, Mysore KS (2005) Insertional mutagenesis: a Swiss Army knife for functional genomics of Medicago truncatula. Trends in Plant Science 10, 229–235.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Tesfaye M, Samac DA, Vance CP (2006) Insights into symbiotic nitrogen fixation in Medicago truncatula. Molecular Plant–Microbe Interactions 19, 330–341.
PubMed |
open url image1

Town CD (2006) Annotating the genome of Medicago truncatula. Current Opinion in Plant Biology 9, 122–127.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Udvardi MK, Tabata S, Parniske M, Stougaard J (2005) Lotus japonicus: legume research in the fast lane. Trends in Plant Science 10, 222–228.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Valot B, Negroni L, Zivy M, Gianinazzi S, Dumas-Gaudot E (2006) A mass spectrometric approach to identify arbuscular mycorrhiza-related proteins in root plasma membrane fractions. Proteomics 6, S145–S155.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

van Rhijn P, Fang Y, Galili S, Shaul O, Atzmon N , et al. (1997) 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. Proceedings of the National Academy of Sciences USA 94, 5467–5472.
Crossref | GoogleScholarGoogle Scholar | open url image1

Vessey KJ, Pawlowski K, Bergman B (2005) Root-based N2-fixing symbioses: legumes, actinorhizal plants, Parasponia sp. and cycads. Plant and Soil 274, 51–78.
Crossref | GoogleScholarGoogle Scholar | open url image1

Vieweg MF, Frühling M, Quandt H-J, Heim U, Bäumlein H, Pühler A, Küster H, Perlick AM (2004) The promoter of the Vicia faba L. leghemoglobin gene VfLb29 is specifically activated in the infected cells of root nodules and in the arbuscule-containing cells of mycorrhizal roots from different legume and nonlegume plants. Molecular Plant–Microbe Interactions 17, 62–69.
PubMed |
open url image1

Vieweg MF, Hohnjec N, Küster H (2005) Two genes encoding different truncated hemoglobins are regulated during root nodule and arbuscular mycorrhiza symbioses of Medicago truncatula. Planta 220, 757–766.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Walter MH, Hans J, Strack D (2002) Two distantly related genes encoding 1-deoxy-d-xylulose 5-phosphate synthases: differential regulation in shoots and apocarotenoid-accumulating mycorrhizal roots. The Plant Journal 31, 243–254.
Crossref | d
-xylulose 5-phosphate synthases: differential regulation in shoots and apocarotenoid-accumulating mycorrhizal roots.&journal=The Plant Journal&volume=31&pages=243-254&publication_year=2002&author=D%20Strack&hl=en&doi=10.1046/j.1365-313X.2002.01352.x" target="_blank" rel="nofollow noopener noreferrer" class="reftools">GoogleScholarGoogle Scholar | PubMed | open url image1

Weidmann S, Sanchez L, Descombin J, Chatagnier O, Gianinazzi S, Gianinazzi-Pearson V (2004) Fungal elicitation of signal transduction-related plant genes precedes mycorrhiza establishment and requires the dmi3 gene in Medicago truncatula. Molecular Plant–Microbe Interactions 17, 1385–1393.
PubMed |
open url image1

Wulf A, Manthey K, Doll J, Perlick AM, Linke B, Bekel T, Meyer F, Franken P, Küster H, Krajinski F (2003) Transcriptional changes in response to arbuscular mycorrhiza development in the model plant Medicago truncatula. Molecular Plant–Microbe Interactions 16, 306–314.
PubMed |
open url image1

Young ND, Cannon SB, Sato S, Kim D, Cook DR, Town CD, Roe BA, Tabata S (2005) Sequencing the genespaces of Medicago truncatula and Lotus japonicus. Plant Physiology 137, 1174–1181.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1