**Author details**

Vladimir A. Zhukov, Oksana Y. Shtark, Alexey Y. Borisov and Igor A. Tikhonovich

\*Address all correspondence to: zhukoff01@yahoo.com

All-Russia Research Institute for Agricultural Microbiology, St.-Petersburg, Russia

## **References**

[1] Vance CP. Symbiotic Nitrogen Fixation and Phosphorus Acquisition. Plant Nutrition in the World of Declining Renewable Resources. Plant Physiol 2001;127(2): 390-397.


plant growth promoting rhizobacteria (PGPR),

We thank Dr. Margarita A. Vishnyakova (N.I. Vavilov All-Russia Research Institute of Plant Industry, St-Petersburg, Russian Federation), Dr. Tatiana S. Naumkina (All-Russia Institute of Legumes and Groat Crops, Orel, Russian Federation) and Dr. Vladimir K. Chebotar ("Bisolbi-Inter" Ltd., St-Petersburg, Russian Federation) for the long-term collaboration in the fields of legume breeding and microbial inocula development. We are also grateful to Victoria Seme‐ nova (Komarov Botanical Institute, St-Petersburg, Russian Federation) for critical reading the manuscript. This work was supported by the grants of RFBR (10-04-00961, 10-04-01146, 12-04-01867), Grant to support leading Russian science school (HIII–337.2012.4) and Govern‐ mental contracts for research with Ministry of Science and Education of Russian Federation

Vladimir A. Zhukov, Oksana Y. Shtark, Alexey Y. Borisov and Igor A. Tikhonovich

All-Russia Research Institute for Agricultural Microbiology, St.-Petersburg, Russia

[1] Vance CP. Symbiotic Nitrogen Fixation and Phosphorus Acquisition. Plant Nutrition in the World of Declining Renewable Resources. Plant Physiol 2001;127(2): 390-397.

\*Address all correspondence to: zhukoff01@yahoo.com

plant-microbe symbioses (PMS),

188 Plant Breeding from Laboratories to Fields

root nodule symbiosis (RNS), root nodule bacteria (rhizobia),

symbiotrophic plant nutrition,

sustainable agriculture,

**Acknowledgements**

(II1304, 16.512.11.2155, #8109).

**Author details**

**References**

systemic regulation

root nodule (RN)

signal interactions,

symbiosomes,


[32] Schüßler A, Schwarzott D, Walker C. A New Fungal Phylum, the Glomeromycota: Phylogeny and Evolution. Mycol Res 2001;105: 1413-1297.

[18] Hirsch AM. Developmental Biology of Legume Nodulation. New Phytol 1992;122:

[19] Sprent JI. Nodulation in Legumes. Royal Botanical Gardens, Kew: Cromwell Press Ltd;

[20] Oke V, Long SR. Bacteroid Formation in the Rhizobium-Legume Symbiosis. Curr Opin

[21] Brewin NJ (1998) Tissue and Cell Invasion by Rhizobium: the Structure and Develop‐ ment of Infection Threads and Symbiosomes. In: Spaink HP, Kondorosi A, Hooykaas PJJ. (eds) The Rhizobiaceae. Molecular Biology of Model Plant-Associated Bacteria.

[22] Tsyganov VE, Voroshilova VA, Herrera-Cervera JA, Sanjuan-Pinilla JM, Borisov AY, Tikhonovich IA, Priefer UB, Olivares J, Sanjuan J. Developmental Down-Regulation of Rhizobial Genes as a Function of Symbiosome Differentiation in Symbiotic Root

[23] Mylona P, Pawlowski K, Bisseling T. Symbiotic Nitrogen Fixation. Plant Cell 1995;7(7):

[24] Pawlowski K, Bisseling T. Rhizobial and Actinorhizal Symbioses: What Are the Shared

[25] Vance CP, Heichel GH. Carbon in N2 Fixation: Limitation or Exquisite Adaptation?

[26] Fedorova M, Tikhonovich IA, Vance CP. Expression of C-assimilating Enzymes in Pea (*Pisum sativum* L.) Root Nodules. In situ Localization in Effective Nodules. Plant Cell

[27] Schubert KR. Products of Biological Nitrogen Fixation in Higher Plants: Synthesis,

[28] Mergaert P, Uchiumi T, Alunni B, Evanno G, Cheron A, Catrice O, Mausset AE, Barloy-Hubler F, Galibert F, Kondorosi A, Kondorosi E. Eukaryotic Control on Bacterial Cell Cycle and Differentiation in the Rhizobium-Legume Symbiosis. Proc Natl Acad Sci

[29] Van de Velde W, Zehirov G, Szatmari A, Debreczeny M, Ishihara H, Kevei Z, Farkas A, Mikulass K, Nagy A, Tiricz H, Satiat-Jeunemaître B, Alunni B, Bourge M, Kucho K, Abe M, Kereszt A, Maroti G, Uchiumi T, Kondorosi E, Mergaert P. Plant Peptides Govern Terminal Differentiation of Bacteria in Symbiosis. Science 2010;327(5969):

[30] Oono R, Denison RF, Kiers ET. Controlling the Reproductive Fate of Rhizobia: How

[31] Oono R, Denison RF. Comparing symbiotic Efficiency Between Swollen Versus

Universal Are Legume Sanctions? New Phytol 2009;183(4): 967-979.

Nonswollen Rhizobial Bacteroids. Plant Physiol 2010;154(3): 1541-1548.

Transport, and Metabolism. Annu Rev Plant Physiol 1986;37: 539-574.

211-237.

190 Plant Breeding from Laboratories to Fields

869-885.

Microbiol 1999;2(6): 641-646.

Dordrecht/Boston/London: Kluwer; 1998. p417-429.

Features? Plant Cell 1996;8(10): 1899-1913.

Annu Rev Plant Physiol 1991;42: 373-392.

Environ 1999;22(10): 1249-1262.

USA 2006;103(13): 5230-5235.

1122-1126.

Nodules of *Pisum sativum* L. New Phytol 2003;159(2): 521-530.

2001.


[62] Harrison MJ, Dewbre GR, Liu J. A Phosphate Transporter from *Medicago truncatula* Involved in the Acquisition of Phosphate Released by Arbuscular Mycorrhizal Fungi. Plant Cell 2002;14: 2413–2429.

[47] Genre A, Bonfante P. Building a Mycorrhiza Cell: How to Reach Compatibility Between

[48] Bieleski RL Phosphate Pools, Phosphate Transport and Phosphate Availability. Annu

[49] Schachtman DP, Reid RJ, Ayling SM. Phosphorus Uptake by Plants: From Soil to Cell.

[50] Tinker PB, Nye PH. Solute Movement in the Rhizosphere. Oxford, UK: Oxford

[51] Neumann E, George E. Nutrient Uptake: The Arbuscular Mycorrhiza Fungal Symbiosis as a Plant Nutrient Acquisition Strategy In: Koltai H, Kapulnik Y (eds) Arbuscular

[52] Smith SE, Smith FA, Jakobsen I. Mycorrhizal Fungi Can Dominate Phosphate Supply to Plants Irrespective of Growth Responses. Plant Physiol 2003;133: 16–20

[53] Schweiger P, Jakobsen I. Laboratory and Field Methods for Measurement Of Hyphal

[54] Nielsen JS, Joner EJ, Declerck S, Olsson S, Jakobsen I. Phospho-Imaging as a Tool for Visualization and Noninvasive Measurement of P Transport Dynamics in Arbuscular

[55] Rufyikiri G, Declerck S, Thiry Y. Comparison of 233U and 33P Uptake and Transloca‐ tion by the Arbuscular Mycorrhizal Fungus *Glomus intraradices* in Root Organ Culture

[56] Ezawa T, Smith SE, Smith FA. P Metabolism and Transport in AM Fungi. Plant Soil

[57] Ashford A. Tubular Vacuoles in Arbuscular Mycorrhizas. New Phytol 2002;54: 545–

[58] Ezawa T, Cavagnaro TR, Smith SE, Smith FA, Ohtomo R. Rapid Accumulation of Polyphosphate in Extraradical Hyphae of an Arbuscular Mycorrhizal Fungus as Revealed by Histochemistry and a Polyphosphate Kinase/Luciferase System. New

[59] Karandashov V, Bucher M. Symbiotic Phosphate Transport in Arbuscular Mycorrhizas.

[60] Balestrini R, Gomez-Ariza J, Lanfranco L, Bonfante P. Laser Microdissection Reveals that Transcripts for Five Plant and One Fungal Phosphate Transporter Genes are Contemporaneously Present in Arbusculated Cells. Molec Plant-Microbe Interact

[61] Javot H, Pumplin N, Harrison MJ. Phosphate in the Arbuscular Mycorrhizal Symbiosis: Transport Properties and Regulatory Roles. Plant Cell Environ 2007;30: 310-322

Uptake of Nutrients in Soil. Plant Soil 2000;226: 237–244.

Mycorrhizas. New Phytol 2002;154: 809–820.

Conditions. Mycorrhiza 2004;14: 203–207.

2002;244: 221–230.

Phytol 2003;161: 387–392.

2007;20: 1055-1062.

Trends Plant Sci 2005;10: 22-29.

547.

Mycorrhizas: Physiology and Function. Dordrecht: Springer; 2010. P 137-167.

Plants and Arbuscular Mycorrhizal Fungi. J Plant Interact 2005;1: 3-13

Rev Plant Physiol 1973;24: 225-252.

Plant Physiol 1998;116: 447-453.

University Press; 2000.

192 Plant Breeding from Laboratories to Fields


[89] Ruiz-Lozano JM, Aroca R. Host Response to Osmotic Stresses: Stomatal Behaviour and Water Use Efficiency of Arbuscular Mycorrhizal Plants. In: Koltai H, Kapulnik Y (eds) Arbuscular Mycorrhizas: Physiology and Function. Dordrecht: Springer; 2010. P 239-256.

[75] Currie AF, Murray PJ, Gange AC. Is a Specialist Root-Feeding Insect Affected by

[76] Harrison MJ. Molecular and Cellular Aspects of the Arbuscular Mycorrhizal Symbiosis.

[77] Blilou I, Bueno P, Ocampo JA, Garcia-Garrido JM. Induction of Catalase And Ascorbate Peroxidase Activities in Tobacco Roots Inoculated with the Arbuscular Mycorrhizal

[78] Blilou I, Ocampo JA, Garcia-Garrido JM. Resistance of Pea Roots to Endomycorrhizal Fungus or *Rhizobium* Correlates with Enhanced Levels of Endogenous Salicylic Acid. J

[79] Lambais MR. Regulation of Plant Defence-Related Genes in Arbuscular Mycorrhizae. In: Podila GK, Douds DD (eds) Current Advances in Mycorrhizae research The

[80] Bonanomi A, Wiemken A, Boller T, Salzer P. Local Induction of a Mycorrhiza-Specific Class III Chitinase Gene in Cortical Root Cells of *Medicago truncatula* Containing

[81] Salzer P, Corbiere H, Boller T. Hydrogen Peroxide Accumulation in *Medicago Trunca‐ tula* Roots Colonized by the Arbuscular Mycorrhiza-Forming Fungus *Glomus mosseae*.

[82] Garcia-Garrido JM, Ocampo JA. Regulation of the Plant Defence Response in Arbus‐

[83] Liu J, Maldonado-Mendoza I, Lopez-Meyer M, Cheung F, Town CD, Harrison MJ. Arbuscular Mycorrhizal Symbiosis is Accompanied by Local and Systemic Alterations in Gene Expression and an Increase in Disease Resistance in the Shoots. Plant J 2007;50:

[84] Bennett AE, Bever JD, Bowers MD. Arbuscular Mycorrhizal Fungal Species Suppress Inducible Plant Responses and Alter Defensive Strategies Following Herbivory.

[85] Kempel A, Schmidt AK, Brandl R, Schadler M. Support from the Underground: Induced Plant Resistance Depends on Arbuscular Mycorrhizal Fungi. Funct Ecol

[86] Quilambo OA. The Vesicular-Arbuscular Mycorrhizal Symbiosis. African J Biotechnol

[87] Augé RM. Water Relations, Drought and Vesicular-Arbuscular Mycorrhizal Symbiosis

[88] Augé RM, Moore JL, Sylvia DM, Cho K. Mycorrhizal Promotion of Host Stomatal Conductance in Relation to Irradiance and Temperature. Mycorrhiza 2004;14: 85-92.

Arbuscular Mycorrhizal Fungi? Appl Soil Ecol 2011;47: 77–83.

American Phytopathological Society, Minnesota; 2000. P 45-59.

Developing or Mature Arbuscules. Plant Biol 2001;3: 94-199.

cular Mycorrhizal Symbiosis. J Exp Bot 2002;53: 377-1386

Ann Rev Plant Physiol Plant Mol Biol 1999;50: 361-389.

Fungus *Glomus mossea.* Mycol Res 2000;104: 722-725.

Exp Bot 1999;50: 1663-1668.

194 Plant Breeding from Laboratories to Fields

Planta 1999;208: 319-325.

Oecologia 2009;160: 711–719.

2010;24: 293–300.

2003;2: 539-546.

Mycorrhiza 2001;11: 3-42.

529-544.


[116] Wu P, Zang G, Ladha JK, McCouch SR, Huang N. Molecular-Marker-Facilitated Investigation on the Ability to Stimulate N2 Fixation in the Rhizosphere by the Irrigated Rice Plants. Theor Appl Genet 1995;91: 1177-1183.

[101] Provorov NA, Vorobyov NI. Evolutionary Genetics of Plant-Microbe Symbioses. New

[102] Shtark O., Provorov N., Mikić A., Borisov A., Ćupina B., Tikhonovich I. Legume Root Symbioses: Natural History and Prospects For Improvement. Ratarstvo i povrtarstvo

[103] Barea JM, Pozo MJ, Azcon R, Azcon-Aguilar C. Microbial Cooperation in the Rhizo‐

[104] Haas D, Defago G. Biological Control of Soil-Borne Pathogens by Fluorescent Pseudo‐ monads. Nature Rev Microbiol. AOP, doi:10.1038/nrmicro1129 (accessed 10 March

[105] Siddiqui ZA. PGPR: Prospective Biocontrol Agents of Plant Pathogens. In: Siddiqui ZA (ed) PGPR: Biocontrol and Biofertilization. Dordrecht: Springer; 2005. P 111–142. [106] Preston GM Plant Perceptions of Plant Growth-Promoting Pseudomonas. Phil Trans R

[107] O'Toole GA, Kolter R. Initiation of Biofilm Formation in *Pseudomonas fluorescens* WCS365 Proceeds via Multiple, Convergent Signalling Pathways: a Genetic Analysis.

[108] Stephens C, Murray W. Pathogen Evolution: How Good Bacteria go Bad. Curr Biol

[109] Catara V. *Pseudomonas corrugata*: Plant Pathogen and/or Biological Resource? Mol Plant

[110] Bolwerk A, Lagopodi AL, Wijfjes AHM, Lamers GEM, Lugtenberg BJJ, Bloemberg GV. Interactions between *Pseudomonas* Biocontrol Strains and *Fusarium oxysporum* f.sp. *radicis-lycopersici* in the Tomato Rhizosphere. In: Tikhonovich IA, Lugtenberg BJJ Provorov NA (eds) Biology of Plant-Microbe Interactions. IS-MPMI, St.-Petersburg

[111] Popova EV, Khatskevich LK. In: Tikhonovich IA, Lugtenberg BJJ Provorov NA (eds) Biology of Plant-Microbe Interactions. IS-MPMI, St.-Petersburg 2004;4: 315-318. [112] Van Loon LC, Bakker PA, Pieterse CMJ. Systemic Resistance Induced by Rhizosphere

[113] Vallad E, Goodman RM. Systemic Acquired Resistance and Induced Systemic Resist‐

[114] Penrose DM, Glick BR. Methods for Isolating and Characterizing ACC Deaminase-Containing Plant Growth-Promoting Rhizobacteria. Physiol Plantarum 2003;118: 10-15.

[115] Glick BR. The Role of Bacterial ACC Deaminase in Promoting the Plant Growth. In: Tikhonovich IA, Lugtenberg BJJ Provorov NA (eds) Biology of Plant-Microbe Interac‐

Bacteria. Annu Rev Phytopathol 1998;36: 453-483.

tions. IS-MPMI, St.-Petersburg 2004;4: 557-560.

ance in Conventional Agriculture. Crop Sci 2004;44: 1920-1934.

York: NOVA Science Publishers; 2010.

(Field and Vegetable Crops Research) 2011;48: 291-304.

sphere. J Exp Botany 2005;56(417): 1761-1778.

Soc Lond B 2004;359: 907-918.

Mol Microbiol 1998;28(3): 449-61.

2001;11: 53-56.

2004;4: 323-326.

Pathol 2007;8: 233-244.

2005).

196 Plant Breeding from Laboratories to Fields


Protein and Oil Content of Different Soybean Cultivars. Russian Agricultural Sciences (Doklady Rossiiskoi Akademii Sel'skohozyaistvennykh Nauk) 2004;4(2): 2-4.

[143] Bakker PAHM, Raaijmakers JM, Bloemberg G et al (eds). New Perspectives and Approaches in Plant Growth-Promoting Rhizobacteria Research (Reprinted from Eur J Plant Pathol 2007;119(2)). Dordrecht: Springer; 2007.

[129] Berg G, Hallmann J. Control of Plant Pathogenic Fungi with Bacterial Endophytes. In: Schulz B, Boyle S, Sieber T (eds) Microbial Root Endophytes. Dordrecht: Springer; 2006.

[130] Kloepper JW, Ryu CM. Bacterial Endophytes as Elicitors of Induced Systemic Resist‐ ance. In: Schulz B, Boyle S, Sieber T (eds) Microbial Root Endophytes. Dordrecht:

[131] Rosenblueth M, Martinez-Romero E. Bacterial Endophytes and their Interactions with

[132] Artursson V, Finlay RD, Jansson JK. Interactions between Arbuscular Mycorrhizal Fungi and Bacteria and Their Potential for Stimulating Plant Growth. Environ Micro‐

[133] Frey-Klett P, Garbaye J, Tarkka M. The Mycorrhiza Helper Bacteria Revisited. New

[134] Garbaye J. Helper Bacteria: a New Dimension to the Mycorrhizal Symbiosis. New

[135] Hildebrandt U, Ouziad F, Marner FJ, Bothe H. The Bacterium *Paenibacillus validus* Stimulates Growth of the Arbuscular Mycorrhizal fungus *Glomus intraradices* up to the

[136] Toljander JF, Lindahl BD, Paul LR, Elfstrand M, Finlay RD. Influence of Arbuscular Mycorrhizal Mycelial Exudates on soil Bacterial Growth and Community Structure.

[137] Rambelli A. The Rhizosphere of Mycorrhizae. In: Marks, G.L., and Koslowski, T.T. (eds)

[138] Ibrahim KK, Arunachalam V, Rao PSK, Tilak KVBR. Seasonal Response of Groundnut Genotypes to Arbuscular Mycorrhiza – *Bradyrhizobium* Inoculation. Microbiol Res

[139] Jacobi LM, Kukalev AS, Ushakov KV, Tsyganov VE, Provorov NA, Borisov AY, Tikhonovich IA. Genetic Variability of Garden Pea (*Pisum sativum* L.) for Symbiotic

[140] Borisov AY, Tsyganov VЕ, Shtark OY, Jacobi LM, Naumkina TS, Serdyuk VP, Vish‐ nyakova MA. Pea (Symbiotic effectiveness). In: Tikhonovich IA, Vishnyakova MA. (eds) The Catalogue of World-Wide Collection. Issue 728. Saint Petersburg: VIR; 2002.

[141] Borisov AY, Shtark OY, Danilova TN, Tsyganov VE, Naumkina TS. Effectiviness of Combined Inoculation of Field Peas with Arbuscular Mycorrhizal Fungi and Nodule Bacteria. Russian Agricultural Sciences (Doklady Rossiiskoi Akademii Sel'skohozyaist‐

[142] Labutova NM, Polyakov AI, Lyakh VA, Gordon VL. Influence of Inoculation with Nodule Bacteria and Endomycorrhizal Fungus *Glomus intraradices* on Yield and Seed

formation of Fertile Spores. FEMS Microbiol Lett 2006;254: 258-267.

Ectomycorrhizae. New York, USA: Academic Press; 1973. P 299–343.

Hosts. Mol Plant-Microbe Interact 2006;19: 827-837.

P 53–70.

198 Plant Breeding from Laboratories to Fields

Springer; 2006. P 33-52.

biol 2006;8(1): 1-10.

Phytol 2007;176: 22–36.

Phytol 1994;128: 197-210.

1995;150: 218-224.

vennykh Nauk) 2004;4: 5-7.

FEMS Microbiol Ecol 2007;61: 295–304.

Capacities. Pisum Genetics 1999;31: 44-45.


and CCaMK Show Functional Conservation Between Two Symbiosis Systems and Constitute the Root of a Common Signaling Pathway. Plant Cell Physiol 2008;49(11): 1659-1671.

[171] Endre G, Kereszt A, Kevei Z, Mihacea S, Kalo P, Kiss GB. A Receptor Kinase Gene Regulating Symbiotic Nodule Development. Nature 2002;417(6892): 962-966.

[156] Handberg K, Stougaard J. *Lotus japonicus*, an Autogamous, Diploid Legume Species for

[157] Barker D, Bianchi S, Blondon F, Dattee Y, Duc G, Essad S, Flament P, Gallusci P, Genier G, Guy P, Muel X, Tourneur J, Denarie J, Huguet T. *Medicago truncatula*, a Model Plant for Studying the Molecular Genetics of the Rhizobium-Legume Symbiosis. Plant Mol

[158] Cook DR. *Medicago truncatula* – a Model in the Making. Curr Opin Plant Biol 1999;2(4):

[159] Young ND, Mudge J, Ellis THN. Legume Genomes: More Than Peas in a Pod. Curr

[160] Cook DR, Vandenbosch K, de Brujin FJ, Huguet T. Model Legumes Get the Nod. Plant

[161] Udvardi MK. Legume Models Strut Their Stuff. Mol Plant Microbe Interact 2001;14(1):

[162] Stougaard J. Genetics and Genomics of Root Symbiosis. Curr Opin Plant Biol 2001;4(4):

[163] Penmetsa RV, Cook DR. A Legume Ethylene-Insensitive Mutant Hyperinfected By Its

[164] Schauser L, Handberg K, Sandal N, Stiller J, Thykjaer T, Pajuelo E, Nielsen A, Stougaard J. Symbiotic Mutants Deficient in Nodule Establishment Identified After T-DNA

[165] Albrecht C, Geurts R, Bisseling T. Legume Nodulation and Mycorrhizae Formation;

[166] Radutoiu S, Madsen LH, Madsen EB, Felle HH, Umehara Y, Gronlund M, Sato S, Nakamura Y, Tabata S, Sandal N, Stougaard J. Plant Recognition of Symbiotic Bacteria

[168] Limpens E, Franken C, Smit P, Willemse J, Bisseling T, Geurts R. LysM-domain Receptor Kinases Regulating Rhizobial Nod Factor-Induced Infection. Science

[169] Op den Camp R, Streng A, De Mita S, Cao Q, Polone E, Liu W, Ammiraju JS, Kudrna D, Wing R, Untergasser A, Bisseling T, Geurts R. LysM-type Mycorrhizal Receptor Recruited for Rhizobium Symbiosis in Nonlegume Parasponia. Science 2011;331(6019):

[170] Banba M, Gutjahr C, Miyao A, Hirochika H, Paszkowski U, Kouchi H, Imaizumi-Anraku H. Divergence of Evolutionary Ways Among Common Sym Genes: CASTOR

Requires Two LysM Receptor-Like Kinases. Nature 2003;425(6958): 585-592. [167] Madsen EB, Madsen LH, Radutoiu S, Olbryt M, Rakwalska M, Szczyglowski K, Sato S, Kaneko T, Tabata S, Sandal N, Stougaard J. A Receptor Kinase Gene of the LysM Type Is Involved in Legume Perception of Rhizobial Signals. Nature 2003;425(6958): 637-640.

Transformation of *Lotus japonicus*. Mol Gen Genet 1998;259(4): 414-423.

Two Extremes in Host Specificity Meet. EMBO J 1999;18(2): 281-288.

Classical and Molecular Genetics. Plant J 1992;2: 487-496.

Rhizobial Symbiont. Science 1997;275(5299): 527-530.

Biol Rep 1990;8: 40-49.

Cell 1997;9: 275-281.

2003;302(5645):630-633.

909-912.

Opin Plant Biol 2003;6(2): 199-204.

301-304.

200 Plant Breeding from Laboratories to Fields

6-9.

328-335.


[192] Kaló P, Gleason C, Edwards A, Marsh J, Mitra RM, Hirsch S, Jakab J, Sims S, Long SR, Rogers J, Kiss GB, Downie JA, Oldroyd GE. Nodulation Signaling in Legumes Requires NSP2, a Member of the GRAS Family of Transcriptional Regulators. Science 2005;308(5729): 1786-1789.

[181] Edwards A, Heckmann AB, Yousafzai F, Duc G, Downie JA. Structural Implications of Mutations in the Pea SYM8 Symbiosis Gene, the DMI1 Ortholog, Encoding a Predicted

[182] Riely BK, Lougnon G, Ané JM, Cook DR. The Symbiotic Ion Channel Homolog DMI1 Is Localized in the Nuclear Membrane of *Medicago truncatula* Roots. Plant J 2007;49(2):

[183] Peiter E, Sun J, Heckmann AB, Venkateshwaran M, Riely BK, Otegui MS, Edwards A, Freshour G, Hahn MG, Cook DR, Sanders D, Oldroyd GE, Downie JA, Ané JM. The *Medicago truncatula* DMI1 Protein Modulates Cytosolic Calcium Signaling. Plant

[184] Kanamori N, Madsen LH, Radutoiu S, Frantescu M, Quistgaard EMH, Miwa H, Downie JA, James EK, Felle HH, Haaning LL, Jensen TH, Sato S, Nakamura Y, Tabata S, Sandal N, Stougaard J. A Nucleoporin Is Required for Induction of Ca2+ Spiking in Legume Nodule Development and Essential for Rhizobial and Fungal Symbiosis. Proc

[185] Saito K, Yoshikawa M, Yano K, Miwa H, Uchida H, Asamizu E, Sato S, Tabata S, Imaizumi-Anraku H, Umehara Y, Kouchi H, Murooka Y, Szczyglowski K, Downie JA, Parniske M, Hayashi M, Kawaguchi M. NUCLEOPORIN85 Is Required for Calcium Spiking, Fungal and Bacterial Symbioses, and Seed Production in *Lotus japonicus*. Plant

[186] Groth M, Takeda N, Perry J, Uchida H, Draxl S, Brachmann A, Sato S, Tabata S, Kawaguchi M, Wang TL, Parniske M. 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 2010;22(7): 2509-2526.

[187] Oldroyd GE, Downie JA. Calcium, Kinases and Nodulation Signalling in Legumes. Nat

[188] Catoira R, Galera C, de Billy F, Penmetsa RV, Journet EP, Maillet F, Rosenberg C, Cook D, Gough C, Denarie J. Four Genes of *Medicago truncatula* Controlling Components of

[189] Gleason C, Chaudhuri S, Yang T, Munoz A, Poovaiah BW, Oldroyd GE. Nodulation Independent of Rhizobia Induced by a Calcium-Activated Kinase Lacking Autoinhi‐

[190] Sanchez L, Weidmann S, Arnould C, Bernard AR, Gianinazzi S, Gianinazzi-Pearson V. *Pseudomonas fluorescens* and *Glomus mosseae* Trigger *DMI3*-Dependent Activation of Genes Related to a Signal Transduction Pathway in Roots of *Medicago truncatula*. Plant

[191] Yano K, Yoshida S, Muller J, Singh S, Banba M, Vicker K. CYCLOPS, a Mediator of Symbiotic Intracellular Accommodation. Proc Natl Acad Sci USA 2008;105(51):

a Nod Factor Transduction Pathway. Plant Cell 2000;12(9): 1647-1665.

Ion Channel. Mol Plant Microbe Interact 2007;20(10): 1183-1191.

208-216.

202 Plant Breeding from Laboratories to Fields

Physiol 2007;145(1): 192-203.

Cell 2007;19(2): 610-624.

Natl Acad Sci USA 2006;103(2): 359-364.

Rev Mol Cell Biol 2004;5(7): 566-576.

bition. Nature 2006;441(7097): 1149-1152.

Physiol 2005;139(2): 1065-1077.

20540-20545.


*Medicago truncatula* and Defines a Highly Conserved, Uncharacterized Plant Gene Family. Plant Physiol 2011;157(1): 328-340.

[215] Catford JG, Staehelin C, Lerat S, Piché Y, Vierheilig H. Suppression of Arbuscular Mycorrhizal Colonization and Nodulation in Split-Root Systems of Alfalfa after Pre-Inoculation and Treatment with Nod Factors. J Exp Bot 2003;54(386): 1481-1487.

[203] Caetano-Anolles G, Gresshoff PM. Plant Genetic Control of Nodulation. Annu Rev

[204] Ferguson BJ, Indrasumunar A, Hayashi S, Lin MH, Lin YH, Reid DE, Gresshoff PM. Molecular Analysis of Legume Nodule Development and Autoregulation. J Integr

[205] Okamoto S, Ohnishi E, Sato S, Takahashi H, Nakazono M, Tabata S, Kawaguchi M. Nod Factor/Nitrate-Induced CLE Genes That Drive HAR1-Mediated Systemic Regulation

[206] Mortier V, Den Herder G, Whitford R, Van de Velde W, Rombauts S, D'Haeseleer K, Holsters M, Goormachtig S. CLE Peptides Control *Medicago truncatula* Nodulation

[207] Krusell L, Madsen LH, Sato S, Aubert G, Genua A, Szczyglowski K, Duc G, Kaneko T, Tabata S,de Bruijn F, Pajuelo E, Sandal N, Stougaard J. Shoot Control of Root Devel‐ opment and Nodulation Is Mediated by a Receptor-Like Kinase. Nature 2002;420(6914):

[208] Nishimura R, Hayashi M, Wu GJ, Kouchi H, Imaizumi-Anraku H, Murakami Y, Kawasaki S, Akao S, Ohmori M, Nagasawa M, Harada K, Kawaguchi M. HAR1 Mediates Systemic Regulation of Symbiotic Organ Development. Nature

[209] Schnabel E, Journet EP, de Carvalho-Niebel F, Duc G, Frugoli J. The *Medicago trunca‐ tula* SUNN Gene Encodes a CLV1-like leucine-Rich Repeat Receptor Kinase That Regulates Nodule Number and Root Length. Plant Mol Biol 2005;58(6):809-822.

[210] Staehelin C, Xie ZP, Illana A, Vierheilig H. Long-Distance Transport of Signals During Symbiosis: Are Nodule Formation and Mycorrhization Autoregulated in a Similar

[211] Nishimura R, Ohmori M, Fujita H, Kawaguchi M. A *Lotus* Basic Leucine Zipper Protein with a RING-Finger Motif Negatively Regulates the Developmental Program of

[212] Oka-Kira E, Tateno K, Miura K, Haga T, Hayashi M, Harada K, Sato S, Tabata S, Shikazono N, Tanaka A, Watanabe Y, Fukuhara I, Nagata T, Kawaguchi M. klavier (klv), a Novel Hypernodulation Mutant of *Lotus japonicus* Affected in Vascular Tissue

[213] Magori S, Oka-Kira E, Shibata S, Umehara Y, Kouchi H, Hase Y, Tanaka A, Sato S, Tabata S, Kawaguchi M. Too Much Love, a Root Regulator Associated with the Long-Distance Control of Nodulation in *Lotus japonicus*. Mol Plant Microbe Interact

[214] Schnabel EL, Kassaw TK, Smith LS, Marsh JF, Oldroyd GE, Long SR, Frugoli JA. The ROOT DETERMINED NODULATION1 Gene Regulates Nodule Number in Roots of

Nodulation. Proc Natl Acad Sci USA 2002;99(23): 15206-15210.

Organization and Floral Induction. Plant J 2005;44(3): 505-515.

Microbiol 1991;45: 345-382.

204 Plant Breeding from Laboratories to Fields

Plant Biol 2010;52(1): 61-76.

422-426.

2002;420(6914): 426-429.

2009;22(3): 259-268.

Way? Plant Signal Behav 2011;6(3): 372-377.

of Nodulation. Plant Cell Physiol 2009;50(1): 67-77.

Locally and Systemically. Plant Physiol 2010;153(1): 222-237.


AJ Valentine, C Elmerich, WE Newton (eds) Biological Nitrogen Fixation: Towards Poverty Alleviation Through Sustainable Agriculture. Proceedings of 15th Internation‐ al Congress on Nitrogen Fixation & 12th International Conference of the African Association for Biological Nitrogen Fixation. Berlin/Heidelberg: Springer Science and Business Media BV; 2008. p15-17.

[238] Bourion V, Rizvi SM, Fournier S, de Larambergue H, Galmiche F, Marget P, Duc G, Burstin J. Genetic Dissection of Nitrogen Nutrition in Pea Through a QTL Approach of Root, Nodule, and Shoot Variability. Theor Appl Genet 2010;121(1): 71-86.

[226] Tikhonovich IA, Provorov NA. Cooperation of Plants and Microorganisms: Getting Closer to the Genetic Construction of Sustainable Agro-Systems. Biotechnol J 2007;2(7):

[227] Shtark OY, Danilova TN, Naumkina TS, Vasilchikov AG, Chebotar VK, Kazakov AE, Zhernakov AI, Nemankin TA, Prilepskaya NA, Borisov AY, Tikhonovich IA. Analysis of Pea (*Pisum sativum* L.) Source Material for Breeding of Cultivars with High Symbiotic Potential and Choice of Criteria for Its Evaluation. Ecological genetics ("Ekologiche‐

[228] Chebotar VK, Kazakov AE, Erofeev SV, Danilova TN, Naumkina TS, Shtark OY, Tikhonovich IA, Borisov AY. Method of Production of Complex Microbial Fertilizer.

[229] Prévost D, Antoun H. Potential Use of Rhizobium as PGPR with Non-Legumes: Abstracts from the Inoculant Forum, March 17-18, 2005. Saskatoon, Saskatchewan,

[230] Hossain MS, Mårtensson A. Potential Use of *Rhizobium* spp. to Improve Fitness of Non-Nitrogen-Fixing Plants. Acta Agriculturae Scandinavica, Section B – Plant Soil Science

[231] Gentili F, Jumpponen A. Potential and Possible Uses of Bacterial and Fungal Biofertil‐ izers. In: Rai MK. (ed.) Handbook of Microbial Biofertilizers. New York: Haworth Press,

[232] Galvan GA, Burger-Meijer K, Kuiper TW, Kik C, Scholten OE. Breeding for Improved Responsiveness to Arbuscular Mycorrhizal Fungi in Onion. Proceedings of 3rd International Congress of the European Integrated Project Quality Low Input Food (QLIF) Congress, Hohenheim, Germany, March 20–23, 2007. (Online) http://

[233] Herridge D, Rose I. Breeding for Enhanced Nitrogen Fixation in Crop Legumes. Field

[235] Graham PH, Hungria M, Tlusty B. Breeding for Better Nitrogen Fixation in Grain Legumes: Where Do the Rhizobia Fit In? Crop Management 2004; doi:10.1094/

[236] Howieson JG, Yates RJ, Foster KJ, Real D, Besier RB. Prospects for the Future Uses of Legumes. In: Dilworth MJ, James EK, Sprent JI, Newton WE. (eds) Nitrogen Fixing Leguminous Symbioses. Berlin/Heidelberg: Springer Science+Business Media BV;

[237] Borisov AY, Danilova TN, Shtark OY, Solovov II, Kazakov AE, Naumkina TS, Vasil‐ chikov AG, Chebotar VK, Tikhonovich IA. Tripartite Symbiotic System of Pea (*Pisum sativum* L.): Applications in Sustainable Agriculture. In: FD Dakora, BM Chimphango,

[234] Rengel Z. Breeding for Better Symbiosis. Plant Soil 2002;245(1): 147-162.

skaja genetika") 2006;4(2): 22-28 (In Russian).

Technology & Engineering; 2006. p1-28.

Crops Res 2000;65: 229-248.

CM-2004-0301-02-RV.

2008. p363-394.

orgprints.org/view/projects/int\_conf\_qlif2007.html

Patent No 2318784. 2008.

2008;58(4): 352-358.

833-848.

206 Plant Breeding from Laboratories to Fields

Canada.

[239] Tominaga A, Gondo T, Akashi R, Zheng SH, Arima S, Suzuki A. Quantitative Trait Locus Analysis of Symbiotic Nitrogen Fixation Activity in the Model Legume *Lotus japonicus*. J Plant Res 2012;125(3): 395-406.
