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Table 1 Genes differentially expressed during organogenic nodule formation in hop.

From: Organogenic nodule development in hop (Humulus lupulus L.): Transcript and metabolic responses

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

  1. 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.