Table 1.
Genes differentially expressed during organogenic nodule formation in hop.
| GenBank Acc. No. | E value | Annotation | 24 h vs 0 | 15d vs 0 | 28d vs 0 | 28d vs 28dWH | Clone ID/contig |
| Defense response, response to stress, response to chemical stimulus, abiotic and biotic stimuli | |||||||
| ES437675 | 1,00E-81 | cationic peroxidase [Nelumbo nucifera] | -3.81 | -1.44 | 2.01 | Hlct1 | |
| ES437719 | 9,00E-119 | peroxidase [Vigna angularis] | 2.73 | 1.53 | 1.79 | 2.03 | Hl4206 |
| ES437713 | 2,00E-87 | peroxidase [Populus trichocarpa] | 2.16 | 1.66 | Hl4578 | ||
| ES437767 | 2,00E-13 | SAG21 (Senescence-Associated Gene 21) [Arabidopsis thaliana] | 1.87 | 2.09 | 1.87 | -1.91 | Hl4571 |
| ES437753 | 4,00E-77 | Senescence-associated [Medicago truncatula] | 4.06 | 4.32 | 3.46 | Hl1471 | |
| ES437674 | 0.0 | M. domestica ribulose-1.5-bisphosphate carboxylase/oxygenase activase | -13.29 | -5.38 | -2.97 | Hlct810 | |
| ES437696 | 1,00E-64 | major allergen Pru p 1 [Prunus persica] | 6.05 | 3.5 | 1.95 | Hl1695 | |
| ES437747 | 2,00E-48 | major allergen Pru p 1 [Prunus persica] | 5.94 | 3.74 | 2.56 | Hlct313 | |
| ES437764 | 2,00E-140 | Solanum tuberosum clone 054G03 Hsp90-2-like mRNA | 2.02 | 2.81 | 3.1 | Hlct1560 | |
| ES437687 | 2,00E-23 | putative gamma-thionin [Castanea sativa] | 5.21 | 1.55 | -1.87 | Hl1925 | |
| ES437729 | 5,00E-20 | mandelonitrile lyase [Arabidopsis thaliana] | -1.46 | NA | 4.06 | Hl2222 | |
| ES437733 | 3,00E-152 | Thiazole biosynthetic enzyme, chloroplast precursor | -3.34 | -3.29 | -2.49 | -2.35 | Hl3328 |
| ES437789 | 2,00E-162 | Humulus lupulus chitinase | 1.74 | 2.52 | 2.38 | Hlct1044 | |
| ES437688 | 1,00E-65 | glutathione S-transferase GST 12 [Glycine max] | 4.2 | 2.63 | 2.62 | Hl1525 | |
| ES437709 | 1,00E-16 | early flowering 3 [Mesembryanthemum crystallinum] | 1.56 | 1.82 | 2.64 | Hl3446 | |
| ES437740 | 1,00E-12 | nematode responsive protein [Arabidopsis thaliana] | 2.64 | 4.57 | 3.12 | Hl4497 | |
| EF624245 | 6,00E-124 | putative phenylalanine ammonia-lyase [Rhizophora mangle] | 1.95 | 1.56 | NA | Hlpal | |
| ES437730 | 3,00E-32 | Populus tremula × Populus tremuloides aux/IAA protein | -1.41 | -1.54 | -2.5 | 2.55 | Hl4491 |
| Macromolecule metabolic processes | |||||||
| ES437720 | 6,00E-10 | Solanum tuberosum extensin | 1.97 | 7.03 | 4.44 | Hlct117 | |
| AY795910 | 0.0 | Humulus lupulus beta-1.3-glucanase | 3.81 | 3.37 | 3.28 | Hlgluc5 | |
| EF593131 | 2,00E-79 | Pectin methylesterase 1 [Pyrus communis] | 1.65 | Hl52 | |||
| ES437689 | 4,00E-121 | Populus tremula xyloglucan endotransglycosylase/hydrolase precursor XTH-30 | 3.48 | 5.3 | 6.87 | Hl3465 | |
| ES437757 | 0.0 | Nicotiana tabacum ZIP | -5.77 | -3.4 | NA | NA | Hl4167 |
| EF624249 | 5,00E-158 | sucrose synthase [Glycine max] | 3.01 | 1.9 | 1.5 | Hlsuc | |
| Cellular metabolic processes | |||||||
| ES437727 | 1,00E-56 | RNA binding [Arabidopsis thaliana] | 2.15 | 2.19 | 2.32 | Hl417 | |
| ES437761 | 4,00E-161 | Avr9/Cf-9 induced kinase 1 [Nicotiana tabacum] | 2.46 | 2.53 | 3.17 | Hl3459 | |
| ES437769 | 6,00E-20 | Plant lipid transfer protein/Par allergen [Medicago truncatula] | 2.66 | 2.71 | 1.76 | Hl3157 | |
| ES437798 | 1,00E-156 | Hevea brasiliensis latex plastidic aldolase-like protein | -9.51 | -4.32 | -2.85 | Hlct77 | |
| ES437772 | 1,00E-94 | ribonuclease/transcriptional repressor [Arabidopsis thaliana] | -1.44 | -2.67 | NA | Hl4319 | |
| ES437711 | 8,00E-81 | pfkB-type carbohydrate kinase family protein, putative expressed [Oryza sativa] | 3.54 | 2.49 | 2.8 | Hl3980 | |
| ES437721 | 0.0 | putative dTDP-glucose 4-6-dehydratase [Arabidopsis thaliana] | NA | 2.07 | 2.23 | Hl4620 | |
| ES437736 | 0.0 | Arabidopsis thaliana mRNA for glyceraldehyde-3-phosphate dehydrogenase C subunit | 2.31 | 2.5 | 1.53 | Hlct23 | |
| ES437788 | 2,00E-152 | fructose-bisphosphate aldolase-like protein [Solanum tuberosum] | NA | 1.91 | -1.87 | Hlct3973 | |
| ES437680 | 6,00E-63 | glyceraldehyde-3-phosphate dehydrogenase A subunit, photosynthetic isoform [Glycine max] | -10.78 | -5.17 | Hl263 | ||
| ES437780 | 6,00E-83 | glycerophosphodiesterase-like protein [Nicotiana tabacum] | -1.6 | -1.58 | 2.65 | Hl3510 | |
| ES437786 | 1,00E-95 | epoxide hydrolase/hydrolase [Arabidopsis thaliana] | NA | 3.18 | Hl1072 | ||
| ES437692 | 0.0 | C. blumei kinetoplast met gene for cobalamine-independent methionine synthase | 3.56 | 2.13 | 1.45 | Hlct4592 | |
| ES437722 | 4,00E-09 | S-adenosylmethionine decarboxylase [Malus × domestica] | NA | NA | 2.6 | NA | Hl3196 |
| ES437681 | 0.0 | Elaeagnus umbellata S-adenosyl-L-methionine synthetase (SAMS2) mRNA | 1.55 | 2.35 | 1.48 | -1.68 | Hlct214 |
| ES437707 | 1,00E-80 | Vitis vinifera 3-deoxy-D-arabino-heptulosonate 7-phosphate synthase | 3.25 | 2.31 | NA | Hl1812 | |
| ES437758 | 3,00E-85 | Capsicum annuum nucleoside diphosphate kinase | 4.72 | 5.1 | 5.03 | Hl1543 | |
| ES437763 | 3,00E-82 | MAP kinase-like protein [Gossypium hirsutum] | -1.89 | -1.66 | -2.08 | 2.48 | Hl4516 |
| ES437718 | 5,00E-58 | Protein kinase; Type I EGF [Medicago truncatula] | -1.46 | -1.62 | -4.38 | 7.51 | Hl4559 |
| ES437766 | 5,00E-77 | Putative phosphatase 2A inhibitor [Arabidopsis thaliana] | -1.68 | -1.92 | -1.67 | 2.35 | Hl2273 |
| Primary metabolic process | |||||||
| ES437723 | 5,00E-11 | Corylus avellana lipid transfer protein precursor | 1.95 | 1.99 | Hl2898 | ||
| ES437779 | 1,00E-14 | Lipoxygenase [Medicago truncatula] | 3.35 | 2.42 | Hllox6 | ||
| ES437705 | 2,00E-31 | Lipoxygenase [Nicotiana attenuata] | -3.26 | 4 | Hl2195 | ||
| Transcription and DNA and RNA metabolism | |||||||
| ES437679 | 2,00E-32 | ZFP4 (ZINC FINGER PROTEIN 4); nucleic acid binding/transcription factor/zinc ion binding [Arabidopsis thaliana] | 3.83 | 2.99 | 3.35 | Hl1813 | |
| ES437796 | 1,00E-43 | histone H2B1 [Gossypium hirsutum] | 2.66 | 2.57 | 2.36 | Hl2418 | |
| ES437677 | 2,00E-62 | A. thaliana histone H4 gene | 3.76 | 1.94 | 1.73 | 2.03 | Hlct2847 |
| Signal transduction | |||||||
| ES437693 | 5,00E-70 | Medicago truncatula small G-protein ROP9 | 6.54 | 7.27 | 6.23 | Hl1506 | |
| ES437706 | 3,00E-118 | Populus tomentosa calmodulin | 1.71 | 2.09 | 1.4 | Hl2815 | |
| Cellular component organization and biogenesis | |||||||
| ES437700 | 1,00E-39 | Gossypium hirsutum RAC-like G-protein Rac1 | 2.04 | 2.02 | 1.98 | Hl1537 | |
| ES437797 | 1,00E-113 | Camellia sinensis alpha tubulin 1 (Tua1) | -5.7 | 7.36 | Hl2210 | ||
| ES437690 | 6,00E-12 | Arabidopsis thaliana POK (POKY POLLEN TUBE) | -8.51 | -2.97 | -1.62 | 1.99 | Hl3610 |
| Protein metabolism | |||||||
| ES437748 | 8,00E-36 | ribosome inactivating protein Euserratin 2 precursor [Euphorbia serrata] | 1.7 | 1.71 | 2.86 | Hl3627 | |
| ES437712 | 6,00E-76 | A. thaliana structural constituent of ribosome (AT5G28060) | 2.82 | 2 | 2.3 | Hl1643 | |
| ES437716 | 5,00E-113 | Cicer arietinum mRNA for ribosomal protein RL5 (rl5 gene) | 3.63 | 5.31 | 5.35 | Hl1520 | |
| ES437765 | 3,00E-57 | structural constituent of ribosome [Arabidopsis thaliana] | -1.44 | 3.03 | Hl3805 | ||
| ES437756 | 5,00E-41 | Triticum aestivum ribosomal protein L39 | 2.8 | 2.54 | 2.2 | Hl4115 | |
| ES437773 | 2,00E-55 | 40S RIBOSOMAL PROTEIN S20 homolog [Arabidopsis thaliana] | 2.85 | NA | 2.29 | NA | Hl1619 |
| ES437744 | 6,00E-56 | ribosomal protein L30 [Lupinus luteus] | 3.72 | 3.71 | 2.83 | Hlct1532 | |
| ES437739 | 3,00E-26 | G. hirsutum mRNA for ribosomal protein 41, large subunit (RL41) | 4.22 | 2.17 | 1.57 | Hlct1769 | |
| ES437701 | 7,00E-15 | putative subtilisin-like serine proteinase [Arabidopsis thaliana] | 1.45 | 1.88 | 2.2 | Hl1547 | |
| ES437775 | 8,00E-18 | Trifolium pratense RNA for putative zinc dependent protease | NA | NA | 2.63 | NA | Hl1923 |
| ES437778 | 3,00E-21 | protein binding/ubiquitin-protein ligase/zinc ion binding [Arabidopsis thaliana] | NA | 1.88 | 2.17 | Hl1495 | |
| ES437685 | 6,00E-25 | ATP binding/protein binding [Arabidopsis thaliana] | -1.47 | -1.62 | -3.24 | 3.09 | Hl2061 |
| Photosynthesis and carbon utilization | |||||||
| ES437710 | 7,00E-165 | oxygen evolving complex 33 kDa photosystem II protein [Nicotiana tabacum] | -10.45 | -4.95 | -2.56 | Hlct484 | |
| ES437702 | 5,00E-88 | Arachis hypogaea photosystem I psaH protein | -7.75 | -4.86 | -2.28 | Hlct829 | |
| ES437794 | 2,00E-46 | photosystem I reaction center subunit × psaK [Nicotiana tabacum] | -6.29 | NA | -2.68 | NA | Hlct526 |
| ES437741 | 0.0 | Glycine max cv. Dare photosystem II type I chlorophyll a/b-binding protein (lhcb1*7) gene | -9.9 | -6.33 | -2.84 | 1.66 | Hlct54 |
| ES437745 | 1,00E-144 | chlorophyll ab binding protein [Gossypium hirsutum], light harvesting complex | -11.69 | -5.89 | -2,43 | 1.86 | Hlct362 |
| ES437704 | 1,00E-95 | photosystem II 23 kDa polypeptide [Nicotiana tabacum] | -7.41 | -4.34 | -1.89 | Hl2435 | |
| ES437703 | 2,00E-131 | chlorophyll a/b binding protein [Solanum tuberosum] | -6.91 | -5.95 | -2.97 | Hlct1969 | |
| ES437759 | 2,00E-07 | LHCII type I chlorophyll a/b binding protein [Vigna radiata] | -18.13 | -8.33 | -3.71 | 1.78 | Hl240 |
| ES437783 | 6,00E-118 | chloroplast pigment-binding protein CP26 [Nicotiana tabacum] | -3.02 | -3.13 | -3.48 | 2.92 | Hl4149 |
| ES437793 | 1,00E-86 | PSI type III chlorophyll a/b-binding protein [Arabidopsis thaliana] | -4.96 | -4.08 | -2.35 | Hl2281 | |
| ES437755 | 3,00E-118 | LHCII type III chlorophyll a/b binding protein [Vigna radiata] | NA | -7.85 | -3.04 | Hl3332 | |
| ES437760 | 5,00E-79 | putative chloroplast chlorophyll a/b-binding protein [Carya cathayensis] | -7.19 | -4.82 | -2.67 | Hl1396 | |
| ES437673 | 7,00E-85 | small subunit ribulose-1.5-bisphosphate carboxylase/oxygenase [Fagus crenata] | -13.36 | -6.44 | -2.49 | Hlct105 | |
| ES437715 | 1,00E-128 | chlorophyll a/b-binding protein CP24 precursor [Vigna radiata] | -7.11 | -5.46 | -2.79 | Hlct1168 | |
| ES437762 | 1,00E-130 | chlorophyll a/b-binding protein [Solanum lycopersicum] | -9.86 | -6.57 | -2.75 | Hlct2446 | |
| ES437697 | 1,00E-74 | Potato mRNA for light inducible tissue-specific ST-LS1 gene | -11.42 | -4.33 | -2.33 | Hlct30 | |
| ES437781 | 4,00E-07 | putative photosystem I reaction centre PSI-D subunit precursor [Solanum tuberosum] | -1.78 | -1.85 | -1.74 | 3.03 | Hl3804 |
| ES437771 | 7,00E-68 | subunit of photosystem I [Cucumis sativus] | -4.84 | -4.02 | -2.08 | Hlct2254 | |
| Generation of precursor metabolites and energy | |||||||
| ES437678 | 7,00E-24 | putative photosystem I reaction center subunit IV [Arabidopsis thaliana] | -4.51 | -3.63 | -1.85 | Hl4247 | |
| ES437751 | 8,00E-87 | Pachysandra terminalis glycolate oxidase | -7.94 | -3.22 | -2.46 | Hl1696 | |
| ES437768 | 2,00E-39 | putative steroid binding protein [Arabidopsis thaliana] | -1.9 | -1.87 | Hl1863 | ||
| ES437752 | 3,00E-62 | F1-ATP synthase delta subunit [Ipomoea batatas] | NA | 2.35 | 2.87 | Hl1512 | |
| ES437695 | 2,00E-138 | Gossypium hirsutum vacuolar H+-ATPase subunit B | 2.52 | 2.82 | 2.8 | Hl3429 | |
| ES437683 | 8,00E-94 | vacuolar-type H+-ATPase (v-ATPase) subunit D [Arabidopsis thaliana] | 1.61 | 1.85 | 2.33 | Hl3612 | |
| Secondary metabolic process | |||||||
| ES437792 | 7,00E-72 | NADPH-protochlorophyllide oxidoreductase [Cucumis sativus] | -4.21 | -3.95 | -2.26 | Hlct395 | |
| ES437754 | 2,00E-173 | Malus × domestica cinnamic acid hydroxylase (C4H1) | 2.03 | 2.24 | 1.67 | Hlct225 | |
| ES437670 | 7,00E-93 | iron ion binding/isopenicillin-N synthase/flavonol synthase [Arabidopsis thaliana] | 2.44 | 5.27 | 2.33 | Hl3668 | |
| Other classes | |||||||
| ES437676 | 1,00E-55 | protein transporter [Arabidopsis thaliana] | -1.47 | -1.84 | -2.25 | 4.29 | Hl1064 |
| ES437750 | 3,00E-22 | Gossypium hirsutum hybrid proline-rich protein 2 | 2.43 | Hlct2443 | |||
| ES437749 | 1,00E-08 | metallothionein 1a [Populus balsamifera subsp. trichocarpa × Populus deltoides] | 1.74 | 2.61 | 2.13 | Hlct1310 | |
| ES437717 | 7,00E-54 | Fagus sylvatica glycine-rich protein 2 | 2.55 | 2.08 | NA | Hl1692 | |
| Unknown function | |||||||
| ES437698 | 3,00E-16 | nectarin IV [Nicotiana langsdorffii × Nicotiana sanderae], xyloglucan-specific fungal endoglucanase-inhibitor | -1.46 | -1.79 | 2.69 | Hl3829 | |
| ES437708 | 2,00E-67 | Stress protein DDR48, related [Medicago truncatula] | 1.65 | 2.22 | 2.9 | Hl3456 | |
| ES437737 | 6,00E-78 | hypothetical protein OsJ_005893 [Oryza sativa], sodium/calcium exchanger protein | 2.11 | 3.17 | 3.52 | Hlct2641 | |
| ES437724 | 2,00E-25 | putative type-1 pathogenesis-related protein [Oryza sativa] | 2.16 | 2.43 | 3.51 | Hl697 | |
| ES437672 | 5,00E-08 | Kunitz inhibitor ST1-like [Medicago truncatula] | 5.39 | 2.28 | 2.95 | Hl2037 | |
| ES437684 | 2,00E-65 | thioredoxin-dependent peroxidase [Nelumbo nucifera] | 1.62 | 2.23 | 1.44 | Hl3152 | |
| ES437732 | 1,00E-28 | cystatin-like protein [Citrus × paradisi] | 1.63 | 1.91 | NA | -1.6 | Hl285 |
| ES437734 | 1,00E-11 | metal ion binding [Arabidopsis thaliana] | -1.5 | -1.77 | 3.84 | Hl3490 | |
| ES437777 | 4,00E-93 | Platanus × acerifolia putative zinc-binding protein | 1.88 | 2.11 | 2.24 | Hl481 | |
| ES437738 | 1,00E-24 | hypothetical protein OsI_022889 [Oryza sativa], AN1-like Zinc finger | 1.98 | 2.27 | Hlct1522 | ||
| ES437774 | 7,00E-28 | S locus F-box protein with the low allelic sequence polymorphism 2-Sf [Prunus mume] | -7.04 | -5.52 | 5.47 | Hl4049 | |
| ES437770 | 3,00E-98 | acireductone dioxygenase-like protein [Brassica juncea] | 1.56 | 2.23 | 1.93 | Hl3444 | |
| ES437691 | 2,00E-31 | auxin-repressed protein-like protein ARP1 [Manihot esculenta] | -10.78 | -1.93 | -1.49 | 2.23 | Hlct188 |
| ES437694 | 2,00E-25 | putative auxin-repressed protein [Prunus armeniaca] | -6.17 | -4.13 | -2.35 | 2.08 | Hl1264 |
| ES437742 | 1,00E-65 | Mannose/glucose-specific lectin | NA | 2.25 | 1.81 | -2.96 | Hl1960 |
| ES437746 | 2,00E-08 | pore-forming toxin-like protein Hfr-2 [Triticum aestivum] | -5.82 | -4.68 | -3.22 | Hlct272 | |
| ES437782 | 4,00E-22 | carbohydrate binding [Arabidopsis thaliana] | -6.94 | -3.46 | -1.57 | Hl2175 | |
| ES437726 | 1,00E-15 | Triticum aestivum acidic ribosomal protein | -2.07 | 2.3 | Hl3792 | ||
| ES437790 | 8E-17 | Similar to threonine endopeptidase [Arabidopsis thaliana] | 5.27 | 7.32 | 5.53 | 2.51 | Hl3859 |
| ES437784 | 7,00E-28 | unknown protein [Arabidopsis thaliana] | 1.8 | 2.16 | 2.87 | Hl3471 | |
| ES437776 | 4,00E-50 | unknown protein [Arabidopsis thaliana] | -2.28 | -2.1 | -2.32 | 2.08 | Hl2053 |
| ES437787 | 4,00E-51 | unknown protein [Arabidopsis thaliana] | 1.58 | -3.72 | -2.41 | 2.82 | Hl3322 |
| No identity | |||||||
| ES437699 | 3.19 | 2.99 | 1.83 | Hl3362 | |||
| ES437682 | 12.98 | 22.04 | 9.41 | Hlct85 | |||
| ES437795 | -1.65 | -3.23 | Hlct367 | ||||
| ES437791 | -1.45 | -1.6 | -1.84 | 2.45 | Hl3793 | ||
| ES437785 | -2.52 | -2.27 | 2.02 | Hl2561 | |||
| ES437735 | -1.65 | 2.01 | Hl1860 | ||||
| ES437731 | 7.52 | 11.15 | 5 | Hlct397 | |||
| ES437686 | 5.78 | 12.48 | 7.98 | 2.59 | Hlct182 | ||
| ES437728 | 2.19 | Hl3941 | |||||
| ES437725 | 1.76 | 1.81 | 2.15 | Hl1453 | |||
| ES437714 | -2.05 | -2.15 | -2.15 | 2.94 | Hl2078 | ||
| ES437671 | -2.61 | -2.13 | -2.46 | Hl393 | |||
| ES437743 | 1.58 | 1.96 | 1.84 | Hl109 | |||
A total of 133 differentially expressed unigenes during different phases of nodule formation were sorted into groups according to their putative physiological role estimated according to TAIR. Clones obtained by a reverse transcriptase–PCR based cloning approach appear in italic. Negative and positive values indicate down- and up-regulation respectively. Values presented in bold format represent those meeting the criteria of a FDR < 0.05 and a fold change ≥ 1.87 or ≤ -1.87. Values without bold format represent a fold change ≥ 1.41 or ≤ -1.41. Note that for the time point T24h versus T0 there are less values in bold format since only two replicates were carried out. NA stands for not available data due to their removal from analysis before normalization.