Register      Login
Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
REVIEW (Open Access)

Medicago truncatula as a model for understanding plant interactions with other organisms, plant development and stress biology: past, present and future

Ray J. Rose
+ Author Affiliations
- Author Affiliations

Australian Research Council Centre of Excellence for Integrative Legume Research, School of Environmental and Life Sciences, The University of Newcastle, Callaghan, NSW 2308, Australia. Email: ray.rose@newcastle.edu.au

Functional Plant Biology 35(4) 253-264 https://doi.org/10.1071/FP07297
Submitted: 17 December 2007  Accepted: 16 April 2008   Published: 3 June 2008

Abstract

Medicago truncatula Gaertn. cv. Jemalong, a pasture species used in Australian agriculture, was first proposed as a model legume in 1990. Since that time M. truncatula, along with Lotus japonicus (Regal) Larsen, has contributed to major advances in understanding rhizobia Nod factor perception and the signalling pathway involved in nodule formation. Research using M. truncatula as a model has expanded beyond nodulation and the allied mycorrhizal research to investigate interactions with insect pests, plant pathogens and nematodes. In addition to biotic stresses the genetic mechanisms to ameliorate abiotic stresses such as salinity and drought are being investigated. Furthermore, M. truncatula is being used to increase understanding of plant development and cellular differentiation, with nodule differentiation providing a different perspective to organogenesis and meristem biology. This legume plant represents one of the major evolutionary success stories of plant adaptation to its environment, and it is particularly in understanding the capacity to integrate biotic and abiotic plant responses with plant growth and development that M. truncatula has an important role to play. The expanding genomic and genetic toolkit available with M. truncatula provides many opportunities for integrative biological research with a plant which is both a model for functional genomics and important in agricultural sustainability.

Additional keywords: abiotic stress, biotic stress, Jemalong 2HA, legumes, nodulation, regeneration.


Acknowledgements

Work in my laboratory on Medicago truncatula has been supported by the Wool Research and Development Corporation, the Grains Research and Development Corporation, The University of Newcastle and currently by an ARC Centre of Excellence Grant for Integrative Legume Research (CILR) to the Universities of Queensland, Melbourne and Newcastle, and the Australian National University (Grant CEO348212). I wish to thank my colleagues from the CILR and my research group for the many stimulating discussions on Medicago truncatula biology; and also Lowell Johnson (KSU) and Ian Kaehne and Andrew Lake (formerly of SARDI) for introducing me to annual Medicago.


References


Alonso JM, Stepanova AN, Leisse TJ, Kim CJ, Chen H , et al. (2003) Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science 301, 653–657.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Amor BB, Shaw SL, Oldroyd GED, Maillet F, Penmetsa RV, Cook D, Long SR, Dénarié J, 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. The Plant Journal 34, 495–506.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Ané J-M, Kiss GB, Riely BK, Penmetsa RV, Oldroyd GED , et al. (2004) Medicago truncatula DMI1 required for bacterial and fungal symbioses in legumes. Science 303, 1364–1367.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Ané J-M, Zhu H, Frugoli J (2008) Recent advances in Medicago truncatula genomics. International Journal of Plant Genomics in press , open url image1

Araújo SS, Duque ASRLA, Santos DMMF, Fevereiro MPS (2004) An efficient transformation method to regenerate a high number of transgenic plants using a new embryogenic line of Medicago truncatula cv. Jemalong. Plant Cell, Tissue and Organ Culture 78, 123–131.
Crossref | GoogleScholarGoogle Scholar | open url image1

Aubert G, Morin J, Jacquin F, Loridon K, Quillet MC, Petit A, Rameau C, Lejeune-Hénaut I, Huguet T, Burnstin J (2006) Functional mapping in pea, as an aid to the candidate gene selection and for investigating synteny with the model legume Medicago truncatula. Theoretical and Applied Genetics 112, 1024–1041.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Axtell MJ, Snyder JA, Bartel DP (2007) Common functions for diverse small RNAs of land plants. The Plant Cell 19, 1750–1769.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Barker DG, Bianchi S, Blondon F, Datteé 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.
Crossref | GoogleScholarGoogle Scholar | open url image1

Benaben V, Duc C, Lefebvre V, Huguet T (1995) TE7, an inefficient symbiotic mutant of Medicago truncatula Gaertn cv Jemalong. Plant Physiology 107, 53–62.
PubMed |
open url image1

Bennett MD, Leitch IJ (1995) Nuclear DNA amounts in angiosperms. Annals of Botany 76, 113–176.
Crossref | GoogleScholarGoogle Scholar | open url image1

Bevan MW, Flavell RB, Chilton MD (1983) A chimaeric antibiotic resistance gene as a selectable marker for plant cell transformation. Nature 304, 184–187.
Crossref | GoogleScholarGoogle Scholar | open url image1

Beveridge CA, Mathesius U, Rose RJ, Gresshoff PM (2007) Common regulatory themes in meristem development and whole plant homeostasis. Current Opinion in Plant Biology 10, 44–51.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Bingham ET, Hurley LV, Kaatz DM, Saunders JW (1975) Breeding alfalfa which regenerates from callus tissue in culture. Crop Science 15, 719–721. open url image1

Bird DMcK (2004) Signaling between nematodes and plants. Current Opinion in Plant Biology 7, 372–376.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Boisson-Dernier A, Chabaud M, Garcia F, Becard G, Rosenberg C, Barker DG (2001) Agrobacterium rhizogenes-transformed roots of Medicago truncatula for the study of nitrogen-fixing and endomycorrhizal symbiotic associations. Molecular Plant–Microbe Interactions 14, 695–700.
Crossref | GoogleScholarGoogle Scholar | 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

Brosnan CA, Mitter N, Christie M, Smith NA, Waterhouse PM, Carroll BJ (2007) Nuclear gene silencing directs reception of long-distance mRNA silencing in Arabidopsis. Proceedings of the National Academy of Sciences USA 104, 14741–14746.
Crossref | GoogleScholarGoogle Scholar | open url image1

Cannon SB, Crow JA, Heuer ML, Wang X, Cannon EKS , et al. (2005) Databases and information integration for the Medicago truncatula genome and transcriptome. Plant Physiology 138, 38–46.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Cannon SB, Sterck L, Rombauts S, Sato S, Cheung F , et al. (2006) Legume genome evolution viewed through the Medicago truncatula and Lotus japonicus genomes. Proceedings of the National Academy of Sciences USA 103, 14959–14964.
Crossref | GoogleScholarGoogle Scholar | open url image1

Carlson PS, Smith HH, Dearing RD (1972) Parasexual interspecific plant hybridisation. Proceedings of the National Academy of Sciences USA 69, 2292–2294.
Crossref | GoogleScholarGoogle Scholar | open url image1

Casimiro I, Beeckman T, Graham N, Bhalerao R, Zhang H, Casero P, Sandberg G, Bennett M (2003) Dissecting Arabidopsis lateral root development. Trends in Plant Science 8, 165–171.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Chabaud M, Larsonneau C, Marmouget C, Huguet T (1996) Transformation of barrel medic (Medicago truncatula Gaertn.) by Agrobacterium tumefaciens and regeneration via somatic embryogenesis of transgenic plants with the MtENOD12 nodulin promoter fused to the gus reporter gene. Plant Cell Reports 15, 305–310. open url image1

Chabaud M, de Carvalho-Niebel F, Barker DG (2003) Efficient transformation of Medicago truncatula cv. Jemalong using the hypervirulent Agrobacterium tumefaciens strain AGL1 Plant Cell Reports 22, 46–51.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Chabaud M , Ratet P , Araújo SS , Duque ASRL , Harrison M , Barker DG (2007) Agrobacterium tumefaciens-mediated transformation and in vitro plant regeneration of M. truncatula. In ‘The Medicago truncatula handbook’. (Eds U Mathesius, E P Journet, LW Sumner). Available at http://www.noble.org/MedicagoHandbook/

Chinchilla D, Zipfel C, Robatzek S, Kemmerling B, Nürnberger T, Jones JDG, Felix G, Boller T (2007) A flagellin-induced complex of the receptor FLS2 and BAK1 initiates plant defence. Nature 448, 497–500.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Choi H-K, Kim D, Uhm T, Limpens E, Lim H , et al. (2004a) A sequence based genetic map of Medicago truncatula and comparison of marker colinearity with M. sativa. Genetics 166, 1463–1502.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Choi H-K, Mun J-H, Kim D-J, Zhu H, Baek J-M , et al. (2004b) Estimating genome conservation between crop and model legume species. Proceedings of the National Academy of Sciences USA 101, 15289–15294.
Crossref | GoogleScholarGoogle Scholar | open url image1

Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. The Plant Journal 16, 735–743.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Cook DR (1999) Medicago truncatula – a model in the making! Current Opinion in Plant Biology 2, 301–304.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Cook DR, VandenBosch K, de Bruijn FJ, Huguet T (1997) Model legumes get the nod. The Plant Cell 9, 275–281.
Crossref | GoogleScholarGoogle Scholar | open url image1

Covitz PA, Smith LS, Long SR (1998) Expressed sequence tags from a root-hair-enriched Medicago truncatula cDNA library. Plant Physiology 117, 1325–1332.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Crane C, Wright E, Dixon RA, Wang Z-Y (2006) Transgenic Medicago truncatula plants obtained from Agrobacterium tumefaciens-transformed roots and Agrobacterium rhizogenes – transformed hairy roots. Planta 223, 1344–1354.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Crawford EJ, Lake AWH, Boyce KG (1989) Breeding annual Medicago species for semiarid conditions in Southern Australia. Advances in Agronomy 42, 399–437. open url image1

Cullimore J, Dénarié J (2003) How legumes select their sweet talking symbionts. Plant Science 302, 575–578. open url image1

de Billy F, Grosjean C, May S, Bennett M, Cullimore JV (2001) Expression studies on AUXI-like genes in Medicago truncatula suggest that auxin is required at two steps in early nodule development. Molecular Plant–Microbe Interactions 14, 267–277.
Crossref | GoogleScholarGoogle Scholar | open url image1

Djemel N, Guedon D, Lechevalier A, Salon C, Miquel M, Prosperi JM, Rochat C, Boutin JP (2005) Development and composition of the seeds of nine genotypes of the Medicago truncatula species complex. Plant Physiology and Biochemistry 43, 557–566.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Ellwood SR, D’Souza NK, Kamphuis LG, Burgess TI, Nair RM, Oliver RP (2006a) SSR analysis of the Medicago truncatula SARDI core collection reveals substantial diversity and unusual genotype dispersal throughout the Mediterranean basin. Theoretical and Applied Genetics 112, 977–983.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Ellwood SR, Kamphuis KL, Oliver RP (2006b) Identification of sources of resistance to Phoma medicaginis isolates in Medicago truncatula SARDI core collection accessions, and multigene differentiation of isolates. Phytopathology 96, 1330–1336.
Crossref | GoogleScholarGoogle Scholar | open url image1

Firnhaber C, Puhler A, Kuster H (2005) EST sequencing and time course microarray hybridisations identify more than 700 M. truncatula genes with developmental expression regulation in flowers and pods. Planta 222, 269–283.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Foster-Hartnett D, Danesh D, Peñuela S, Sharopova N, Endre G, Vandenbosch KA, Young ND, Samac DA (2007) Molecular and cytological responses of Medicago truncatula to Erysiphe pisi. Molecular Plant Pathology 8, 307–319.
Crossref | GoogleScholarGoogle Scholar | open url image1

Fraley RT, Rogers SB, Horsch RB, Sanders PR, Flick JS , et al. (1983) Expression of bacterial genes in plant cells. Proceedings of the National Academy of Sciences USA 80, 4803–4807.
Crossref | GoogleScholarGoogle Scholar | open url image1

Galibert F, Finan TM, Long SR, Puhler A, Abola P , et al. (2001) The composite genome of the legume symbiont Sinorhizobium meliloti. Science 293, 668–672.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Gallardo K, Le Signor C, Vandekerckhove J, Thompson RD, Burstin J (2003) Proteomics of Medicago truncatula seed development establishes the time frame of diverse metabolic processes related to reserve accumulation. Plant Physiology 133, 664–682.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Gao L-L, Anderson JP, Klingler JP, Nair RM, Edwards OR, Singh KB (2007) Involvement of the octadecanoid pathway in bluegreen aphid resistance in Medicago truncatula. Molecular Plant–Microbe Interactions 20, 82–93.
Crossref | GoogleScholarGoogle Scholar | open url image1

Gao L-L, Klingler JP, Anderson JP, Edwards OR, Singh KB (2008) Characterization of pea aphid resistance in Medicago truncatula. Plant Physiology 146, 996–1009.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Garcês HMP, Champagne CEM, Townsley BT, Park S, Malhó R, Pedroso MC, Harada JJ, Sinha NR (2007) Evolution of asexual reproduction in leaves of the genus Kalanchoë. Proceedings of the National Academy of Sciences USA 104, 15578–15583.
Crossref | GoogleScholarGoogle Scholar | open url image1

Gaulin E, Jacquet C, Bottin A, Dumas B (2007) Root rot disease of legumes caused by Aphanomyces eutiches. Molecular Plant Pathology 8, 539–548.
Crossref | GoogleScholarGoogle Scholar | open url image1

Gleason C, Chaudhuri S, Yang T, Muñoz A, Poovaiah BW, Oldroyd GED (2006) Nodulation independent of rhizobia induced by a calcium-activated kinase lacking autoinhibition. Nature 441, 1149–1152.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Gonzalez-Rizzo S, Crespi M, Frugier F (2006) The Medicago truncatula CRE1 cytokinin receptor regulates lateral root development and early symbiotic interaction with Sinorhizobium meliloti The Plant Cell 18, 2680–2693.
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

Hecht V, Vielle-Calzada JP, Hartog MV, Schmidt EDL, Boutilier K, Grossniklaus U, de Vries SC (2001) The Arabidopsis somatic embryogenesis receptor kinase 1 gene is expressed in developing ovules and embryos and enhances embryogenic competence in culture. Plant Physiology 127, 803–816.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Herrera-Estrella LA, Depicker M, van Montagu M, Schell J (1983) Expression of chimaeric genes transferred into plant cells using a Ti-plasmid-derived vector. Nature 303, 209–213.
Crossref | GoogleScholarGoogle Scholar | open url image1

Hirota A, Kato K, Fukaki H, Aida M, Tasaka M (2007) The Auxin-regulated AP2/EREBP gene PUCHI is required for morphogenesis in the early lateral root primordium of Arabidopsis. The Plant Cell 19, 2156–2168.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Hoffmann B, Trinh TH, Leung J, Kondorosi A, Kondorosi E (1997) A new Medicago truncatula line with superior in vitro regeneration, transformation, and symbiotic properties isolated through cell culture selection. Molecular Plant–Microbe Interactions 10, 307–315.
Crossref | GoogleScholarGoogle Scholar | open url image1

Hohnjec N, Henckel K, Bekel T, Gouzy J, Dondrup M, Goesmann A, Küster H (2006) Transcriptional snapshots provide insights into the molecular basis of arbuscular mycorrhiza in the model legume Medicago truncatula. Functional Plant Biology 33, 737–748.
Crossref | GoogleScholarGoogle Scholar | open url image1

Imin N, de Jong F, Mathesius U, van Noorden G, Saeed NA, Wang X-D, Rose RJ, Rolfe BG (2004) Proteome reference maps of Medicago truncatula embryogenic cell cultures generated from single protoplasts. Proteomics 4, 1883–1896.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Imin N, Nizamidin M, Daniher D, Nolan KE, Rose RJ, Rolfe BG (2005) Proteomic analysis of somatic embryogenesis in Medicago truncatula. Explant cultures grown under 6-Benzylaminopurine and 1-Naphthaleneacetic acid treatments. Plant Physiology 137, 1250–1260.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Imin N, Nizamidin M, Wu T, Rolfe BG (2007) Factors involved in root formation in Medicago truncatula. Journal of Experimental Botany 58, 439–451.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Javot H, Penmetsa RV, Terzaghi N, Cook DR, Harrison MJ (2007) A Medicago truncatula transporter indispensable for the arbuscular mycorrhizal symbiosis. Proceedings of the National Academy of Sciences USA 104, 1720–1725.
Crossref | GoogleScholarGoogle Scholar | open url image1

Jayasena KW, Hajimorad MR, Law EG, Rehman A-U, Nolan KE, Zanker T, Rose RJ, Randles JW (2001) Resistance to Alfalfa mosaic virus in transgenic barrel medic lines containing the virus coat protein gene. Australian Journal of Agricultural Research 52, 67–72.
Crossref | GoogleScholarGoogle Scholar | open url image1

Johnson LB, Stuteville DL, Higgins RK, Skinner DZ (1981) Regeneration of alfalfa plants from protoplasts of selected Regen S clones. Plant Science Letters 20, 297–304.
Crossref | GoogleScholarGoogle Scholar | open url image1

Jones-Rhoades MW, Bartel DP, Bartel B (2006) MicroRNAs and their regulatory roles in plants. Annual Review of Plant Biology 57, 19–53.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Kaló P, Gleason C, Edwards A, Marsh J, Mitra RM , et al. (2005) Nodulation signaling in legumes requires NSP2, a member of the GRAS family of transcriptional regulators. Science 308, 1786–1789.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Klingler J, Creasy R, Gao L, Nair RM, Calix AS, Jacob HS, Edwards OR, Singh KB (2005) Aphid resistance in Medicago truncatula involves antixenosis and phloem-specific, inducible antibiosis and maps to a single locus flanked by NBS-LRR resistance gene analogs. Plant Physiology 137, 1445–1455.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Klingler JP, Edwards OR, Singh KB (2006) Independent action and contrasting phenotypes of resistance genes against spotted alfalfa aphid and bluegreen aphid in Medicago truncatula. New Phytologist 173, 630–640.
Crossref |
open url image1

Kulikova O, Gualtieri G, Geurts R, Kim D-J, Cook D, Huguet T, de Jong JH, Fransz PF, Bisseling T (2001) Integration of the FISH pachytene and genetic maps of Medicago truncatula. The Plant Journal 27, 49–58.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Kulikova O, Geurts R, Lamine M, Kim DJ, Cook DR, Leunissen J, de Jong H, Roe BA, Bisseling T (2004) Satellite repeats in the functional centromere and pericentromeric heterochromatin of Medicago truncatula. Chromosoma 113, 276–283.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Lake AWH (1989) Spotted alfalfa aphid survival and reproduction on annual medics with various levels of aphid resistance. Australian Journal of Agricultural Research 40, 117–123.
Crossref | GoogleScholarGoogle Scholar | open url image1

Lévy J, Bres C, Geurts R, Chalhoub B, Kulikova O , et al. (2004) A putative Ca2+ and calmodulin-dependent protein kinase required for bacterial and fungal symbioses. Science 303, 1361–1364.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Limpens E, Mirabella R, Fedorova E, Franken C, Franssen H, Bisseling T, Geurts R (2005) Formation of organelle-like N2-fixing symbiosomes in legume root nodules is controlled by DM12. Proceedings of the National Academy of Sciences USA 102, 10375–10380.
Crossref | GoogleScholarGoogle Scholar | 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 G, Penuela 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

Loi A, Nutt BJ, McRobb R, Ewing MA (2000) Potential new alternative annual pasture legumes for Australian Mediterranean farming system. Cahiers Options Méditerranéennes 45, 51–54. open url image1

Loi A, Howieson JG, Nutt BJ, Carr SJ (2005) a second generation of annual pasture legumes and their potential for inclusion in Mediterranean-type farming systems. Australian Journal of Experimental Agriculture 45, 289–299.
Crossref | GoogleScholarGoogle Scholar | open url image1

Malamy JE (2005) Intrinsic and environmental response pathways that regulate root system architecture. Plant, Cell & Environment 28, 67–77.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Mantiri FR, Kurdyukov S, Lohar DP, Sharopova N, Saeed NA, Wang X-D, VandenBosch KA, Rose RJ (2008) The transcription factor MtSERF1 of the ERF subfamily identified by transcriptional profiling is required for somatic embryogenesis induced by auxin plus cytokinin in Medicago truncatula. Plant Physiology 146, 1622–1636.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Mathesius U (2003) Conservation and divergence of signalling pathways between roots and soil microbes – the Rhizobium-legume symbiosis compared to the development of lateral roots, mycorrhizal interactions and nematode induced galls. Plant and Soil 255, 105–119.
Crossref | GoogleScholarGoogle Scholar | open url image1

Mathesius U, Keijzers G, Natera SH, Weinman JJ, Djordjevic MA, Rolfe BG (2001) Establishment of a root proteome reference map for the model legume Medicago truncatula using the expressed sequence tag database for peptide mass fingerprinting. Proteomics 1, 1424–1440.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Merchan F, de Lorenzo L, Rizzo SG, Niebel A, Manyani H, Frugier F, Souse C, Crespi M (2007) Identification of regulatory pathways involved in the reacquisition of root growth after salt stress in Medicago truncatula. The Plant Journal 51, 1–17.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Middleton PH, Jakab J, Penmetsa RV, Starker CG, Doll J , et al. (2007) An ERF transcription factor in Medicago truncatula that is essential for nod factor signal transduction. The Plant Cell 19, 1221–1234.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Millar AH, Heazlewood JL, Kristensen BK, Braun H-P, Møller IM (2005) The plant mitochondrial proteome. Trends in Plant Science 10, 36–43.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Murai N, Sutton DW, Murray MG, Slightom JL, Merlo DJ , et al. (1983) Phaseolin gene from bean is expressed after transfer to sunflower via tumor-inducing plasmid vectors. Science 222, 476–482.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Murray JD, Karas BJ, Sato S, Tabata S, Amyot L, Szczyglowski K (2007) A cytokinin perception mutant colonized by Rhizobium in the absence of nodule organogenesis. Science 315, 101–104.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Nakano T, Suzuki K, Fujimura T, Shinshi H (2006) Genome-wide analysis of the ERF gene family in Arabidopsis and rice. Plant Physiology 140, 411–432.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Nam Y-W, Penmetsa RV, Endre G, Uribe P, Kim D, Cook DR (1999) Construction of a bacterial artificial chromosome library of Medicago truncatula and identification of clones containing ethylene-response genes. Theoretical and Applied Genetics 98, 638–646.
Crossref | GoogleScholarGoogle Scholar | open url image1

Nolan KE, Rose RJ (1998) Plant regeneration from cultured Medicago truncatula with particular reference to abscisic acid and light treatments. Australian Journal of Botany 46, 151–160.
Crossref | GoogleScholarGoogle Scholar | open url image1

Nolan KE, Rose RJ, Gorst JE (1989) Regeneration of Medicago truncatula from tissue culture: increased somatic embryogenesis from regenerated plants. Plant Cell Reports 8, 278–281.
Crossref | GoogleScholarGoogle Scholar | open url image1

Nolan KE, Irwanto RR, Rose RJ (2003) Auxin up-regulates MtSERK1 expression in both Medicago truncatula root-forming and embryogenic cultures. Plant Physiology 133, 218–230.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Oldroyd GED (2007) Nodules and hormones. Science 315, 52–53.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Oldroyd GED, Downie JA (2006) Nuclear calcium changes at the core of symbiosis signalling. Current Opinion in Plant Biology 9, 351–357.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Parniske M (2004) Molecular genetics of the arbuscular mycorrhizal symbiosis. Current Opinion in Plant Biology 7, 414–421.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Penmetsa RV, Cook DR (1997) A legume ethylene-insensitive mutant hyperinfected by its rhizobial symbiont. Science 275, 527–530.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Penmetsa RV, Cook DR (2000) Production and characterization of diverse developmental mutants of Medicago truncatula. Plant Physiology 123, 1387–1397.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Pii Y, Crimi M, Cremonese G, Spena A, Pandolfini T (2007) Auxin and nitric oxide control indeterminate nodule formation. BMC Plant Biology 7, 21.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Potters G, Pasternak TP, Guisez Y, Palme KJ, Jansen MAK (2007) Stress-induced morphogenic responses: growing out of trouble? Trends in Plant Science 12, 98–105.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Prayitno J, Rolfe BG, Mathesius U (2006) The ethylene-insensitive sickle mutant of Medicago truncatula shows altered auxin transport regulation during nodulation. Plant Physiology 142, 168–180.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Ratet P , Porcedu A , Tadege M , Mysore KS (2006) Insertional mutagenesis in Medicago truncatula using Tnt1 retrotransposon. In ‘The Medicago truncatula handbook’. (Eds U Mathesius, EP Journet, LW Sumner) Available at http://www.noble.org/MedicagoHandbook/

Riely BK, Ané J-M, Penmetsa RV, Cook DR (2004) Genetic and genomic analysis in model legumes bring Nod-factor signalling to center stage. Current Opinion in Plant Biology 7, 408–413.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Rose RJ, Nolan KE (1995) Regeneration of Medicago truncatula from protoplasts isolated from kanamycin-sensitive and kanamycin-resistant plants. Plant Cell Reports 14, 349–354.
Crossref | GoogleScholarGoogle Scholar | open url image1

Rose RJ, Nolan KE (2006) Genetic regulation of somatic embryogenisis with particular reference to Arabidopsis thaliana and Medicago truncatula. In Vitro Cellular & Developmental Biology - Plant 42, 473–481. open url image1

Rose RJ, Johnson LB, Kemble RJ (1986) Restriction endonuclease studies on the chloroplast and mitochondrial DNAs of alfalfa (Medicago sativa L.) protoclones. Plant Molecular Biology 6, 331–338.
Crossref | GoogleScholarGoogle Scholar | open url image1

Rose RJ, Nolan KE, Bicego L (1999) The development of the highly regenerable seed line Jemalong 2HA for transformation of Medicago truncatula – implications for regenerability via somatic embryogenesis. Journal of Plant Physiology 155, 788–791. open url image1

Rose RJ , Nolan KE , Niu C (2003) Genetic transformation of Medicago species. In ‘Applied genetics of Leguminosae biotechnology’. (Eds PK Jaiwal, RP Singh) pp. 223–237. (Kluwer Academic Publishers: Dordrecht, The Netherlands)

Rose RJ, Wang X-D, Nolan KE, Rolfe BG (2006) Root meristems in Medicago truncatula tissue culture arise from vascular-derived procambial-like cells in a process regulated by ethylene. Journal of Experimental Botany 57, 2227–2235.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Sagan M, Morandi D, Tarenghi E, Duc G (1995) Selection of nodulation and mycorrhizal mutants in the model plant Medicago truncatula (Gaertn.) after γ-ray mutagenesis. Plant Science 111, 63–71.
Crossref | GoogleScholarGoogle Scholar | open url image1

Salzer P, Bonanomi A, Beyer K, Vögeli-Lange R, Aeschbacher RA, Lange J, Wiemken A, Kim D, Cook DR, Boller T (2000) Differential expression of eight chitinase genes during mycorrhiza formation, nodulation and pathogen infection. Molecular Plant–Microbe Interactions 13, 763–777.
Crossref | GoogleScholarGoogle Scholar | open url image1

Samac DA, Graham MA (2007) Recent advances in legume-microbe interactions: recognition, defense resonse, and symbiosis from a genomic perspective. Plant Physiology 144, 582–587.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Saunders J, Bingham ET (1972) Production of alfalfa plants from callus tissue. Crop Science 12, 804–808. open url image1

Schmidt EDL, Guzzo F, Toonen MAJ, de Vries SC (1997) A leucine-rich repeat containing receptor-like kinase marks somatic plant cells competent to form embryos. Development 124, 2049–2062.
PubMed |
open url image1

Schnabel E, Journet E-P, de Carvalho-Niebel F, Duc G, Frugoli J (2005) The Medicago truncatula SUNN gene encodes a CLV1-like leucine-rich repeat receptor kinase that regulates nodule number and root length. Plant Molecular Biology 58, 809–822.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Shaver JM, Oldenburg DJ, Bendich AJ (2008) The structure of chloroplast DNA molecules and the effect of light on the amount of chloroplast DNA during development in Medicago truncatula. Plant Physiology 146, 1064–1074.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Sheahan MB, McCurdy DW, Rose RJ (2005) Mitochondria as a connected population: ensuring continuity of the mitochondrial genome during plant cell dedifferentiation through massive mitochondrial fusion. The Plant Journal 44, 744–755.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Skoog F, Miller CO (1957) Chemical regulation of growth and organ formation in plant tissue cultured in vitro. Symposia of the Society for Experimental Biology 11, 118–131. open url image1

Smit P, Raedts J, Portyanko V, Debellé F, Gough C, Bisseling T, Geurts R (2005) NSP1 of the GRAS protein family is essential for rhizobial Nod factor-induced transcription. Science 308, 1789–1791.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Somerville CR, Ogren WL (1979) A phosphoglycolate phosphatase-deficient mutant of Arabidopsis. Nature 280, 833–836.
Crossref | GoogleScholarGoogle Scholar | open url image1

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

Tesfaye M, Silverstein KAT, Bucciarelli B, Samac DA, Vance CP (2006) The Affymetrix Medicago GeneChip array is applicable for transcript analysis of alfalfa (Medicago sativa) Functional Plant Biology 33, 783–788.
Crossref | GoogleScholarGoogle Scholar | open url image1

Thatcher LF, Anderson JP, Singh KB (2005) Plant defence response: what have we learnt from Arabidopsis? Functional Plant Biology 32, 1–19.
Crossref | GoogleScholarGoogle Scholar | open url image1

The Genome Initiative (2000) Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408, 796–815.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Thomas MR, Rose RJ, Nolan KE (1992) Genetic transformation of Medicago truncatula using Agrobacterium with genetically modified Ri and disarmed Ti plasmids. Plant Cell Reports 11, 113–117.
Crossref | GoogleScholarGoogle Scholar | open url image1

Thoquet P, Ghérardi M, Journet E-P, Kereszt A, Ané J-M, Prosperi J-M, Huguet T (2002) The molecular genetic linkage map of the model legume Medicago truncatula: an essential tool for comparative legume genomics and the isolation of agronomically important genes. BMC Plant Biology 2, 1.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Tian D, Rose RJ (1999) Asymmetric somatic hybridisation between the annual legumes Medicago truncatula and Medicago scutellata. Plant Cell Reports 18, 989–996.
Crossref | GoogleScholarGoogle Scholar | open url image1

Tirichine L, Imaizumi-Anraku H, Yoshida S, Murakami Y, Madsen LH , et al. (2006) Deregulation of a Ca2+/calmodulin-dependent kinase leads to spontaneous nodule development. Nature 441, 1153–1156.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Tirichine L, Sandal N, Madsen LH, Radutoiu S, Albreksten AS, Sato S, Asamizu E, Tabata S, Stougaard J (2007) A gain-of-function mutation in a cytokinin receptor triggers spontaneous root nodule organogenesis. Science 315, 104–107.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Tivoli B, Baranger A, Sivasithamparam K, Barbetti MJ (2006) Annual Medicago: from a model crop challenged by a spectrum of necrotrophic pathogens to a model plant to explore the nature of disease resistance. Annals of Botany 98, 1117–1128.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Trieu AT, Harrison MJ (1996) Rapid transformation of Medicago truncatula regeneration via shoot organogenesis. Plant Cell Reports 16, 6–11.
Crossref | GoogleScholarGoogle Scholar | open url image1

Tucker MR, Araujo A-CG, Paech NA, Hecht V, Schmidt EDL, Rossell J-B, de Vries SC, Koltunow AMG (2003) Sexual and apomictic reproduction in Hieracium subgenus Pilosella are closely interrelated developmental pathways. The Plant Cell 15, 1524–1537.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Udvardi MK, Scheible W-R (2005) GRAS genes and the symbiotic green revolution. Science 308, 1749–1750.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Udvardi MK, Kakar K, Wandrey M, Montanari O, Murray J , et al. (2007) Legume transcription factors: global regulators of plant development and response to the environment. Plant Physiology 144, 538–549.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Vailleau F, Sartorel E, Jardinaud MF, Chardon F, Genin S, Huguet T, Gentzbittel L, Petitprez M (2007) Characterization of the interaction between the bacterial wilt pathogen Ralstonia solanacearum and the model legume plant Medicago truncatula. Molecular Plant–Microbe Interactions 20, 159–167.
Crossref | GoogleScholarGoogle Scholar | open url image1

Wang JH, Rose RJ, Donaldson BI (1996) Agrobacterium-mediated transformation and expression of foreign genes in Medicago truncatula. Australian Journal of Plant Physiology 23, 265–270. open url image1

Wang H, Chen J, Wen J, Tadege M, Li G, Liu Y, Mysore KM, Ratet P, Chen R (2008) Control of compound leaf development by FLORICAULA/LEAFY ortholog SINGLE LEAFLET1 in Medicago truncatula. Plant Physiology 146, 1759–1772.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Watson BS, Asirvatham VS, Wang L, Sumner LW (2003) Mapping the proteome of barrel medic (Medicago truncatula). Plant Physiology 131, 1104–1123.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Weeks JT, Ye J, Rommens CM (2008) Development of an in planta method for transformation of alfalfa (Medicago sativa). Transgenic Research in press ,
PubMed |
open url image1

Weerasinghe RR, Bird DM, Allen NS (2005) Root-knot nematodes and bacterial Nod factors elicit common signal transduction events in Lotus japonicus. Proceedings of the National Academy of Sciences USA 102, 3147–3152.
Crossref | GoogleScholarGoogle Scholar | open url image1

Young ND, Mudge J, Ellis THN (2003) Legume genomes: more than peas in a pod. Current Opinion in Plant Biology 6, 199–204.
Crossref | GoogleScholarGoogle Scholar | 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

Zhang J-Y, Broeckling CD, Blancaflor EB, Sledge MK, Sumner LW (2005) Overexpression of WXP1, a putative Medicago truncatula AP2 domain-containing transcription factor gene, increases cuticular wax accumulation and enhances drought tolerance in transgenic alfalfa (Medicago sativa). The Plant Journal 42, 689–707.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Zhou X, Chandrasekharan MB, Hall TC (2004) High rooting frequency and functional analysis of GUS and GFP expression in transgenic Medicago truncatula A17. New Phytologist 162, 813–822.
Crossref | GoogleScholarGoogle Scholar | open url image1