Cell- and Tissue-Specific Transcriptome Analyses of Medicago truncatula Root Nodules

PLoS ONE

Volumn 8, Issue 5, 2013, Pages

  Limpens, Erik ^a   Moling, Sjef ^a   Hooiveld, Guido ^a   Pereira, Patrícia A ^b   Bisseling, Ton ^a   Becker, Jörg D ^b   Küster, Helge ^c  

^a WAGENINGEN UNIVERSITY   (Netherlands)

^b INSTITUTO GULBENKIAN DE CIÊNCIA   (Portugal)

^c LEIBNIZ UNIVERSITY HANNOVER   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; BARREL MEDIC; CELL SPECIFICITY; CONTROLLED STUDY; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENE MAPPING; GENETIC SELECTION; LASER CAPTURE MICRODISSECTION; MERISTEM; NITROGEN FIXATION; NODULATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PLANT CELL; RHIZOBIUM; SYMBIONT; TISSUE SPECIFICITY; TRANSCRIPTOMICS; VALIDATION PROCESS;

GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, PLANT; HOST-PATHOGEN INTERACTIONS; IN SITU HYBRIDIZATION; LASER CAPTURE MICRODISSECTION; MEDICAGO TRUNCATULA; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PLANT ROOTS; ROOT NODULES, PLANT; SINORHIZOBIUM MELILOTI; SYMBIOSIS;

MEDICAGO; MEDICAGO TRUNCATULA; RHIZOBIUM;

EID: 84878426818     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0064377     Document Type: Article

References (101)

1. Roth LE, Stacey G, (1989) Bacterium release into host cells of nitrogen-fixing soybean nodules: the symbiosome membrane comes from three sources. Eur J Cell Biol 49: 13-23.
2. Oldroyd GE, Murray JD, Poole PS, Downie JA, (2011) The rules of engagement in the legume-rhizobial symbiosis. Annul Rev Genet 45: 119-144.
3. Kouchi H, Imaizumi-Anraku H, Hayashi M, Hakoyama T, Nakagawa T, et al. (2010) How many peas in a pod? Legume genes responsible for mutualistic symbioses underground. Plant Cell Physiol 51: 1381-1397.
4. Emons AMC, Mulder BM, (2000) How the deposition of cellulose microfibrils builds cell wall architecture. Trends Plant Sci 5: 35-40.
5. Jones KM, Kobayashi H, Davies BW, Taga ME, Walker GC, (2007) How rhizobial symbionts invade plants: The Sinorhizobium-Medicago model. Nat Rev Microbiol 5: 619-633.
6. Timmers AC, Auriac MC, de Billy F, Truchet G, (1998) Nod factor internalization and microtubular cytoskeleton changes occur concomitantly during nodule differentiation in alfalfa. Development 125: 339-349.
7. Vasse J, de Billy F, Camut S, Truchet G, (1990) Correlation between ultrastructural differentiation of bacteroids and nitrogen fixation in Alfalfa nodules. J Bacteriol 172: 4295-4306.
8. Brewin NJ, (2004) Plant cell wall remodelling in the Rhizobium-legume symbiosis. Crit Rev Plant Sci 23: 293-316.
9. Limpens E, Ivanov S, van Esse W, Voets G, Fedorova E, et al. (2009) Medicago N2-fixing symbiosomes acquire the endocytic identity marker Rab7 but delay the acquisition of vacuolar identity. Plant Cell 21: 2811-2828.
10. Mergeart P, Uchiumi T, Alunni B, Evanno G, Cheron A, et al. (2006) Eukaryotic control on bacterial cell cycle and differentiation in the Rhizobium-legume symbiosis. Proc Natl Acad Sci USA 103: 5230-5235.
11. Van de Velde W, Zehirov G, Szatmari A, Debreczeny M, Ishihara H, et al. (2010) Plant peptides govern terminal differentiation of bacteria in symbiosis. Science 327: 1122-1126.
12. Soupène E, Foussard M, Boistard P, Truchet G, Batut J, (1995) Oxygen as a key developmental regulator of Rhizobium meliloti N2-fixation gene expression within the alfalfa root nodule. Proc Natl Acad Sci USA 92: 3759-3763.
13. Ott T, van Dongen JT, Gunther C, Krusell L, Desbrosses G, et al. (2005) Symbolic leghemoglobins are crucial for nitrogen fixation in legume root nodules but not for general plant growth and development. Curr Biol 15: 531-535.
14. White J, Prell J, James EK, Poole P, (2007) Nutrient sharing between symbionts. Plant Physiol 144: 604-614.
15. Van de Velde W, Guerra JC, De Keyser A, De Rycke R, Rombauts S, et al. (2006) Aging in legume symbiosis. A molecular view on nodule senescence in Medicago truncatula. Plant Physiol 141: 711-720.
16. Gamas P, de Carvalho Niebel F, Lescure N, Cullimore JV, (1996) Use of a substrative hybridization approach to indentify new Medicago truncatula genes induced during root nodule development. Mol Plant Microbe Interact 9: 233-242.
17. Küster H, Hohnjec N, Krajinski F, El YF, 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. J Biotechnol 108: 95-113.
18. Mitra RM, Long SR, (2004) Plant and bacterial symbiotic mutants define three transcriptionally distinct stages in the development of the Medicago truncatula/Sinorhizobium meliloti symbiosis. Plant Physiol 134: 595-604.
19. Lohar DP, Sharopova N, Endre G, Penuela S, Samac D, et al. (2006) Transcript analysis of early nodulation events in Medicago truncatula. Plant Physiol 140: 221-234.
20. El Yahyaoui F, Kuster H, Ben Amor B, Hohnjec N, Puhler 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 Physiol 136: 3159-3176.
21. Godiard L, Niebel A, Micheli F, Gouzy J, Ott T, et al. (2007) Identification of new potential regulators of the Medicago truncatula-Sinorhizobium meliloti symbiosis using a large-scale suppression subtractive hybridization approach. Mol Plant Microbe Interact 20: 321-332.
22. Benedito VA, Torres-Jerez I, Murray JD, Andriankaja A, Allen S, et al. (2008) A gene expression atlas of the model legume Medicago truncatula. Plant J 55: 504-513.
23. Manthey K, Krajinski F, Hohnjec N, Firnhaber C, Pühler A, et al. (2004) Transcriptome profiling in root nodules and arbuscular mycorrhiza identifies a collection of novel genes induced during Medicago truncatula root endosymbioses. Mol Plant Microbe Interact 17: 1063-1077.
24. Høgslund N, Radutoiu S, Krusell L, Voroshilova V, Hannah MA, et al. (2009) Dissection of symbiosis and organ development by integrated transcriptome analysis of Lotus japonicus mutant and wild-type plants. PLoS One 4: e6556.
25. Czaja LF, Hogekamp C, Lamm P, Maillet F, Martinez EA, et al. (2012) Transcriptional responses toward diffusible signals from symbiotic microbes reveal MtNFP- and MtDMI3-dependent reprogramming of host gene expression by arbuscular mycorrhizal fungal lipochitooligosaccharides. Plant Physiol 159: 1671-1685.
26. Maunoury N, Redondo-Nieto M, Bourcy M, Van de Velde W, Alunni B, et al. (2011) Differentiation of symbiotic cells and endosymbionts in Medicago truncatula nodulation are coupled to two transcriptome-switches. Plos One 5: e9519.
27. Moreau S, Verdenaud M, Ott T, Letort S, de Billy F, et al. (2011) Transcription reprogramming during root nodule development in Medicago truncatula. PLoS One 6: e16463.
28. Schnable PS, Hochholdinger F, Nakazono M, (2004) Global expression profiling applied to plant development. Curr Opin Plant Biol 7: 50-56.
29. Kerk NM, Ceserani T, Tausta SL, Sussex IM, Nelson TM, (2003) Laser capture microdissection of cells from plant tissues. Plant Physiol 132: 27-35.
30. Hogekamp C, Arndt D, Pereira PA, Becker JD, Hohnjec N, et al. (2011) Laser microdissection unravels cell-type-specific transcription in arbuscular mycorrhizal roots, including CAAT-box transcription factor gene expression correlating with fungal contact and spread. Plant Physiol 157: 2023-2043.
31. Gamas P, de Billy F, Truchet G, (1998) Symbiosis-specific expression of two Medicago truncatula nodulin genes, MtN1 and MtN13, encoding products homologous to plant defense proteins. Mol Plant Microbe Interact 11: 393-403.
32. de Carvalho Niebel F, Lescure N, Cullimore JV, Gamas P, (1998) The Medicago truncatula MtAnn1 gene encoding an annexin is induced by Nod factors and during the symbiotic interaction with Rhizobium meliloti. Mol Plant Microbe Interact 11: 504-513.
33. Mathis R, Grosjean C, de Billy F, Huguet T, Gamas P, (1999) The early nodulin gene MtN6 is a novel marker for events preceding infection of Medicago truncatula roots by Sinorhizobium meliloti. Mol Plant Microbe Interact 12: 544-555.
34. Journet EP, El-Gachtouli N, Vernoud V, de Billy F, Pichon M, et al. (2001) Medicago truncatula ENOD11: a novel RPRP-encoding early nodulin gene expressed during mycorrhization in arbuscule-containing cells. Mol Plant Microbe Interact 14: 737-748.
35. Combier JP, Vernié T, de Billy F, El Yahyaoui F, Mathis R, et al. (2007) The MtMMPL1 early nodulin is a novel member of the matrix metalloendoproteinase family with a role in Medicago truncatula infection by Sinorhizobium meliloti. Plant Physiol 144: 703-716.
36. Vernié T, Moreau S, de Billy F, Plet J, Combier JP, et al. (2008) EFD Is an ERF transcription factor involved in the control of nodule number and differentiation in Medicago truncatula. Plant Cell 20: 2696-2713.
37. Wang D, Griffitts J, Starker C, Fedorova E, Limpens E, et al. (2010) A nodule-specific protein secretory pathway required for nitrogen-fixing symbiosis. Science 327: 1126-1129.
38. Cebolla A, Vinardell JM, Kiss E, Oláh B, Roudier F, et al. (1999) The mitotic inhibitor ccs52 is required for endoreduplication and ploidy-dependent cell enlargement in plants. EMBO J 18: 4476-4484.
39. Foucher F, Kondorosi E, (2000) Cell cycle regulation in the course of nodule organogenesis in Medicago. Plant Mol Biol 43: 773-786.
40. Lauber MH, Waizenegger I, Steinmann T, Schwarz H, Mayer U, et al. (1997) The Arabidopsis KNOLLE protein is a cytokinesis-specific syntaxin. J Cell Biol. 139: 1485-1493.
41. Fung TK, Poon RY, (2005) A roller coaster ride with the mitotic cyclins. Semin Cell Dev Biol 16: 335-42.
42. Osipova MA, Mortier V, Demchenko KN, Tsyganov VE, Tikhonovich IA, et al. (2012) Wuschel-related homeobox5 gene expression and interaction of CLE peptides with components of the systemic control add two pieces to the puzzle of autoregulation of nodulation. Plant Physiol 158: 1329-1341.
43. Limpens E, Mirabella R, Fedorova E, Franken C, Franssen H, et al. (2005) Formation of organelle-like N2-fixing symbiosomes in legume root nodules is controlled by DMI2. Proc Natl Acad Sci USA 102: 10375-10380.
44. Pislariu CI, Dickstein R, (2007) An IRE-like AGC kinase gene, MtIRE, has unique expression in the invasion zone of developing root nodules in Medicago truncatula. Plant Physiol 144: 682-694.
45. Vernoud V, Journet EP, Barker D, (1999) MtENOD20, a Nod factor-inducible molecular marker for root cortical cell activation. Mol Plant Microbe Interact 12: 604-614.
46. Kevei Z, Vinardell JM, Kiss GB, Kondorosi A, Kondorosi E, (2002) Glycine-rich proteins encoded by a nodule-specific gene family are implicated in different stages of symbiotic nodule development in Medicago spp. Mol Plant Microbe Interact 15: 922-931.
47. Godiard L, Lepage A, Moreau S, Laporte D, Verdenaud M, et al. (2011) MtbHLH1, a bHLH transcription factor involved in Medicago truncatula nodule vascular patterning and nodule to plant metabolic exchanges. New Phytol 191: 391-404.
48. Dickstein R, Hu X, Yang J, Ba L, Coque L, et al. (2002) Differential expression of tandemly duplicated Enod8 genes in Medicago. Plant Sci 163: 333-343.
49. Fortin MG, Morrison NA, Verma DP, (1987) Nodulin-26, a peribacteroid membrane nodulin is expressed independently of the development of the peribacteroid compartment. Nucleic Acids Res 15: 813-824.
50. Hohnjec N, Lenz F, Fehlberg V, Vieweg MF, Baier MC, et al. (2009) The signal peptide of the Medicago truncatula modular nodulin MtNOD25 operates as an address label for the specific targeting of proteins to nitrogen-fixing symbiosomes. Mol Plant Microbe Interact 22: 63-72.
51. Krusell L, Krause K, Ott T, Desbrosses G, Krämer U, et al. (2005) The sulfate transporter SST1 is crucial for symbiotic nitrogen fixation in Lotus japonicus root nodules. Plant Cell 17: 1625-1636.
52. Mergaert P, Nikovics K, Kelemen Z, Maunoury N, Vaubert D, et al. (2003) A novel family in Medicago truncatula consisting of more than 300 nodule-specific genes coding for small, secreted polypeptides with conserved cysteine motifs. Plant Physiol 132: 161-173.
53. Liu J, Miller SS, Graham M, Bucciarelli B, Catalano CM, et al. (2006) Recruitment of novel calcium-binding proteins for root nodule symbiosis in Medicago truncatula. Plant Physiol 141: 197-177.
54. Andriankaja A, Boisson-Dernier A, Frances L, Sauviac L, Jauneau A, et al. (2007) AP2-ERF transcription factors mediate Nod factor dependent MtENOD11 activation in root hairs via a novel cis-regulatory motif. Plant Cell 19: 2866-2885.
55. 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. Plant Cell 19: 1221-1234.
56. Sharma SB, Signer ER, (1990) Temporal and spatial regulation of the symbiotic genes of Rhizobium meliloti in planta revealed by transposon Tn5-gusA. Genes Dev 4: 344-356.
57. Schlaman HR, Horvath B, Vijgenboom E, Okker RJ, Lugtenberg BJ, (1991) Suppression of nodulation gene expression in bacteroids of Rhizobium leguminosarum biovar viciae. J Bacteriol 173: 4277-4287.
58. Marie C, Plaskitt KA, Downie JA, (1994) Abnormal bacteroid development in nodules induced by glucosamine synthase mutant of Rhizobium leguminosarum. Mol Plant-Microbe Interact 7: 482-487.
59. Xie F, Murray JD, Kim J, Heckmann AB, Edwards A, et al. (2012) Legume pectate lyase required for root infection by rhizobia. Proc Natl Acad Sci USA 109: 633-638.
60. Miyahara A, Richens J, Starker C, Morieri G, Smith L, et al. (2010) Conservation in function of a SCAR/WAVE component during infection thread and root hair growth in Medicago truncatula. Mol Plant Microbe Interact 23: 1553-1562.
61. Hossain MS, Liao J, James EK, Sato S, Tabata S, et al. (2012) Lotus japonicus ARPC1 is required for rhizobial infection. Plant Physiol 160: 917-928.
62. Davidson AL, Newcomb W, (2001) Changes in actin microfilament arrays in developing pea root nodule cells. Can J Bot 79: 767-776.
63. Gaude N, Bortfeld S, Duensing N, Lohse M, Krajinski F, (2012) Arbuscule-containing and non-colonized cortical cells of mycorrhizal roots undergo extensive and specific reprogramming during arbuscular mycorrhizal development. Plant J 69: 510-528.
64. Maillet F, Poinsot V, Andre O, Puech-Pages V, Haouy A, et al. (2011) Fungal lipochitooligosaccharide symbiotic signals in arbuscular mycorrhiza. Nature 469: 58-63.
65. Op den Camp R, Streng A, De Mita S, Cao Q, Polone E, et al. (2011) LysM-type mycorrhizal receptor recruited for Rhizobium symbiosis in nonlegume parasponia. Science 331: 909-912.
66. Pislariu CI, Dickstein R, (2007) The AGC Kinase MtIRE: A Link to Phospholipid Signaling During Nodulation? Plant Signal Behav 2: 314-316.
67. Deyoung BJ, Clark SE, (2008) BAM receptors regulate stem cell specification and organ development through complex interactions with CLAVATA signaling. Genetics 180: 895-904.
68. Mortier V, Den Herder G, Whitford R, Van de Velde W, Rombauts S, et al. (2010) CLE peptides control Medicago truncatula nodulation locally and systemically. Plant Physiol 153: 222-237.
69. Kurakawa T, Ueda N, Maekawa M, Kobayashi K, Kojima M, et al. (2007) Direct control of shoot meristem activity by a cytokinin-activating enzyme. Nature 445: 652-655.
70. Ané JM, Kiss GB, Riely BK, Penmetsa RV, Oldroyd GE, et al. (2004) Medicago truncatula DMI1 required for bacterial and fungal symbioses in legumes. Science 30: 1364-1367.
71. Peiter E, Sun J, Heckmann AB, Venkateshwaran M, Riely BK, et al. (2007) The Medicago truncatula DMI1 protein modulates cytosolic calcium signaling. Plant Physiol 145: 192-203.
72. Messinese E, Mun JH, Yeun LH, Jayaraman D, Rougé P, et al. (2007) A novel nuclear protein interacts with the symbiotic DMI3 calcium- and calmodulin-dependent protein kinase of Medicago truncatula. Mol. Plant-Microbe Interact 20: 912-921.
73. Ovchinnikova E, Journet EP, Chabaud M, Cosson V, Ratet P, et al. (2011) IPD3 controls the formation of nitrogen-fixing symbiosomes in pea and Medicago Spp. Mol Plant Microbe Interact 24: 1333-1344.
74. Smit P, Raedts J, Portyanko V, Debellé F, Gough C, et al. (2005) NSP1 of the GRAS protein family is essential for rhizobial Nod factor-induced transcription. Science 308: 1789-1791.
75. Prell J, White JP, Bourdes A, Bunnewell S, Bongaerts RJ, et al. (2009) Legumes regulate Rhizobium bacteroid development and persistence by the supply of branched-chain amino acids. Proc Natl Acad Sci USA 106: 12477-12482.
76. Jahn TP, Møller AL, Zeuthen T, Holm LM, Klaerke DA, et al. (2004) Aquaporin homologues in plants and mammals transport ammonia. FEBS Lett 574: 31-36.
77. Galinha C, Hofhuis H, Luijten M, Willemsen V, Blilou I, et al. (2007) PLETHORA proteins as dose-dependent master regulators of Arabidopsis root development. Nature 449: 1053-1057.
78. Péret B, De Rybel B, Casimiro I, Benková E, Swarup R, et al. (2009) Arabidopsis lateral root development: an emerging story. Trends Plant Sci 14: 399-408.
79. Ferguson BJ, Reid JB, (2005) Cochleata: getting to the root of legume nodules. Plant Cell Physiol 46: 1583-1589.
80. Couzigou JM, Zhukov V, Mondy S, Abu El Heba G, Cosson V, et al. (2012) NODULE ROOT and COCHLEATA Maintain Nodule Development and Are Legume Orthologs of Arabidopsis BLADE-ON-PETIOLE Genes. Plant Cell 24: 4498-4510.
81. Grunewald W, van Noorden G, Van Isterdael G, Beeckman T, Gheysen G, et al. (2009) Manipulation of auxin transport in plant roots during Rhizobium symbiosis and nematode parasitism. Plant Cell 21: 2553-2562.
82. Fukaki H, Tameda S, Masuda H, Tasaka M, (2002) Lateral root formation is blocked by a gain-of-function mutation in the SOLITARY-ROOT/IAA14 gene of Arabidopsis. Plant J 29: 153-168.
83. Vanneste S, De Rybel B, Beemster GT, Ljung K, De Smet I, et al. (2005) Cell cycle progression in the pericycle is not sufficient for SOLITARY ROOT/IAA14-mediated lateral root initiation in Arabidopsis thaliana. Plant Cell 17: 3035-3050.
84. Okushima Y, Overvoorde PJ, Arima K, Alonso JM, Chan A, et al. (2005) Functional genomic analysis of the AUXIN RESPONSE FACTOR gene family members in Arabidopsis thaliana: unique and overlapping functions of ARF7 and ARF19. Plant Cell 17: 444-463.
85. Chen LQ, Hou BH, Lalonde S, Takanaga H, Hartung ML, et al. (2010) Sugar transporters for intercellular exchange and nutrition of pathogens. Nature 468: 527-532.
86. Shi L, Twary SN, Yoshioka H, Gregerson RG, Miller SS, (1997) Nitrogen assimilation in alfalfa: isolation and characterization of an aspargine synthetase gene showing enhanced expression in root nodules and dark-adapted leaves. Plant Cell 9: 1339-1356.
87. Thimm O, Bläsing O, Gibon Y, Nagel A, Meyer S, et al. (2004) MAPMAN: a user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes. Plant J 2004 37: 914-939.
88. Porta H, Rueda-Benítez P, Campos F, Colmenero-Flores JM, Colorado JM, et al. (1999) Analysis of lipoxygenase mRNA accumulation in the common bean (Phaseolus vulgaris L.) during development and under stress conditions. Plant Cell Physiol 40: 850-858.
89. Wisniewski JP, Gardner CD, Brewin NJ, (1999) Isolation of lipoxygenase cDNA clones from pea nodule mRNA. Plant Mol Biol 39: 775-783.
90. Pozo MJ, Van Loon LC, Pieterse CMJ, (2005) Jasmonates - Signals in plant-microbe interactions. J Plant Growth Regul 23: 211-222.
91. Nakagawa T, Kawaguchi M, (2006) Shoot-applied MeJA suppresses root nodulation in Lotus japonicus. Plant Cell Physiol 47: 176-180.
92. Sun J, Cardoza V, Mitchell DM, Bright L, Oldroyd G, et al. (2006) Crosstalk between jasmonic acid, ethylene and Nod factor signaling allows integration of diverse inputs for regulation of nodulation. Plant J 46: 961-970.
93. Hause B, Schaarschmidt S, (2009) The role of jasmonates in mutualistic symbioses between plants and soil-born microorganisms. Phytochemistry 70: 1589-15899.
94. Combier JP, Frugier F, de Billy F, Boualem A, El-Yahyaoui F, et al. (2006) MtHAP2-1 is a key transcriptional regulator of symbiotic nodule development regulated by microRNA169 in Medicago truncatula.Genes Dev. 20: 3084-3088.
95. Limpens E, Ramos J, Franken C, Raz V, Compaan B, et al. (2004) RNA interference in Agrobacterium rhizogenes-transformed roots of Arabidopsis and Medicago truncatula. J Exp Bot 55: 983-992.
96. Gentleman RC, Carey VJ, Bates DM, Bolstad B, Dettling M, et al. (2004) Bioconductor: open software development for computational biology and bioinformatics. Genome Biol 5: R80.
97. Liu W, Kohlen W, Lillo A, Op den Camp R, Ivanov S, et al. (2011) Strigolactone biosynthesis in Medicago truncatula and rice requires the symbiotic GRAS-type transcription factors NSP1 and NSP2. Plant Cell 23: 3853-3865.
98. Sartor MA, Tomlinson CR, Wesselkamper SC, Sivaganesan S, Leikauf GD, et al. (2006) Intensity-based hierarchical Bayes method improves testing for differentially expressed genes in microarray experiments. BMC Bioinformatics 7: 538.
99. Storey JD, Tibshirani R, (2003) Statistical significance for genome wide studies. Proc Natl Acad Sci USA 100: 9440-9445.
100. Op den Camp R, De Mita S, Lillo A, Cao Q, Limpens E, et al. (2011) A phylogenetic strategy based on a legume-specific whole genome duplication yields symbiotic cytokinin type-A response regulators. Plant Physiol 157: 2013-2022.
101. van de Wiel C, Scheres B, Franssen H, van Lierop MJ, van Lammeren A, et al. (1990) The early nodulin transcript ENOD2 is located in the nodule parenchyma (inner cortex) of pea and soybean root nodules. EMBO J 9: 1-7.