DOI 10.1007/s10142-016-0510-3
ORIGINAL ARTICLE
Abstract Strawberry is an ideal model for studying the molecular biology of the development and ripening of nonclimacteric fruits. Hormonal regulation of gene expression
along all these processes in strawberries is still to be fully
elucidated. Although auxins and ABA have been pointed
out as the major regulatory hormones, few high-throughput
analyses have been carried out to date. The role for ethylene
and gibberellins as regulatory hormones during the development and ripening of the strawberry fruit remain still elusive.
By using a custom-made and high-quality oligo microarray
platform done with over 32,000 probes including all of the
genes actually described in the strawberry genome, we have
analysed the expression of genes during the development and
ripening in the receptacles of these fruits. We classify these
Enriqueta Moyano-Caete
bb2mocae@uco.es
Laura Medina-Puche
b22mepul@uco.es
Rosario Blanco-Portales
bb2blpor@uco.es
Antonio Rodrguez-Franco
arfranco@uco.es
Abbreviations
ABA
Abscisic acid
Ct
Threshold cycle
EST
Expressed sequence tag
G1
Green1 development stage
G3
Green3 development stage
GAs
Gibberellins
GO
Gene ontology
IAA
Indole-3-acetic acid
MEP
2-C-methyl-D-erithritol 4-phosphate pathway
MVA
Mevalonate pathway
NCED
9-cis-Epoxycarotenoid dioxygenase
NDGA
Nordihydroguaiaretic acid
qRTQuantitative real-time-polymerase chain reaction
PCR
R
Red ripe ripening stage
TFs
Transcription factors
Tm
Melting temperature
u.a.i
Arbitrary units of intensity
Introduction
Fruit developing and ripening process is determinated by numerous factors including light, hormones, temperature and
genotype. Fruits can be classified as climacteric or non-climacteric, depending upon the presence or not of a burst in
respiration taking place at the onset of ripening. In climacteric
fruits, such as tomato, it is well known that the plant hormone
ethylene triggers the ripening process (Giovannoni 2001;
Giovannoni 2004; Giovannoni 2007; Klee and Giovannoni
2011). Grapes and strawberries, however, are two model nonclimacteric fruits where the role of ethylene and other plant
hormones in fruit development and ripening remains still uncertain (Chervin et al. 2004; Symons et al. 2006; Symons et al.
2012; Bttcher et al. 2013; Kuhn et al. 2014; Fortes et al. 2015).
Like many other fleshy fruits, the strawberry undergoes
four sequential stages. The first stage includes organogenesis
that involves fertilization and ovary development (fruit set).
The second stage is an active process of cell division accompanied by seed and early embryo formation (Wechter et al.
2008). In the third phase, fruit growth is produced by cell
expansion until large vacuolated cells are formed that make
up the flesh of the fruits. Cell expansion includes changes in
the cell wall structure and continuous accumulation in vacuoles of carbohydrate, organics acids and different compounds
that help to retain the osmotic pressure and the flow of water
into expanding cells (Wechter et al. 2008). The fourth is
the ripening phase that takes place after seed maturation
and is characterized by a rise in the content of soluble
solids in receptacles, a conversion of starch to sugars,
the production of natural aroma and flavour compounds,
alterations to fruit shape, size, texture and pigmentation
and a partial degradation of cell walls that lead to an
increased susceptibility to post-harvest pathogens
(Wechter et al. 2008). Most of these structural, biochemical and physiological events occurring in the fruit
receptacle are putatively regulated by hormones.
The hormonal control of the ripening of strawberry
(Fragaria ananassa) is starting to be revealed. It has been
proposed that both ABA and auxins are heavily involved in
the development of this fruit (Perkins-Veazie 1995; MedinaPuche et al. 2014). Auxins, synthesized by the immature
achenes, seem to promote receptacle cell division and expansion and at the same time prevent ripening, so the removal of
achenes in immature fruits or the application of auxins synthesis inhibitors leads to dwarf fruits and to the premature
expression of many ripening-related genes (Medina-Escobar
et al. 1997; Trainotti et al. 1999; Redondo-Nevado et al. 2001;
Bentez-Burraco et al. 2003; Cumplido-Laso et al. 2012;
Daminato et al. 2013; Molina-Hidalgo et al. 2013, 2015;
Medina-Puche et al. 2014, 2015). ABA seems to play a major
role once the fruits have already developed in size. The endogenous content of ABA increases substantially at the final
stages of fruit ripening, and this was accompanied by the
induction of many ripening-related genes including those involved in anthocyanin production (Koyama et al. 2010; Chai
et al. 2011; Chen et al. 2011; Jia et al. 2011; Daminato et al.
2013; Molina-Hidalgo et al. 2013; Medina-Puche et al. 2014).
Therefore, the addition of ABA synthesis inhibitors such as
NDGA fully blocks the ripening process, whereas water deprivation, which is known to increase endogenous ABA biosynthesis, promotes premature ripening (Medina-Puche et al.
2014). However, other ABA-independent pathways could also
mediate some aspects of the receptacle ripening process (Jia
et al. 2013).
Some other plant hormones as ethylene or gibberellins seem
also to play minor roles in the ripening of strawberry. Along
the ripening, a very low level of ethylene compared with standard climacteric fruits is produced (Perkins-Veazie 1995;
Leshem and Pinchasov 2000). This low concentration of ethylene is present in green fruits, decay in white fruits and eventually increase at the red stage of ripening (Perkins-Veazie et al.
1996; Iannetta et al. 2006). Although the application of ethylene to strawberry fruits does not have important effects on
ripening process, it affects the expression of a subset of
ripening-related genes as -galactosidase, pectin methyl
Fig. 1 Transcriptomic analysis performed between different strawberry tissues in several experimental situations
genes whose expression was not affected by auxins, suggesting that other hormones or regulatory signals (e.g. ABA,
brassinosteroids and/or gibberellins) could be involved in this
process. In fact, a recent transcriptomic study performed in
strawberry has identified 41 unigenes whose expression was
regulated only by ABA (Chen et al. 2015).
Table 1
genes
Ripening regulation
Cluster
Number of genes
R-up
UP(ABA+AUX-)
UP(ABA+AUX0)
UP(ABA0AUX-)
369
116
356
UP(ABA0AUX0)
Total R-up
R-down
DOWN(ABA0AUX+)
DOWN(ABA-AUX+)
DOWN(ABA-AUX0)
DOWN(ABA0AUX0)
Total R-down
Total differentially expressed 1805
440
1281
338
6
133
47
524
value). GO terms were assigned to a total of 1335 sequences (aprox. 74 %) (Tables S7S14), whereas 470
remained non-annotated possibly due to either a lack of
homologous sequences or the presence of non-coding
RNA in the population of analysed genes.
GO terms distribution at level 2 is summarized in pie charts
(Fig. S1). An enrichment for GO terms related to aroma, flavonols, biotic stress and ABA/ethylene hormones was found
during the fruit ripening process (R-up) whereas photosynthetic apparatus and auxin-related GO terms were present
mainly during the fruit development process (R-down). We
detected a similar enrichment in cell wall-related GO terms
Recently, Chen et al. (2015) have also described the induction of some of these genes, such as pectate lyase and
Putave funcon
the total signal intensity for each feature on the microarray platform.
Gene ID in purple indicates specifity of expression in ripe receptacle
against to vegetative tissues
p-value
Up regulated
a.u.i.
Reference
CLUSTER UP(ABA+AUX-)
gene27724
gene22294
gene34010
gene34009
gene23453
gene07931
gene01341
gene19765
gene13476
gene28407
gene06565
gene32435
gene03054
gene15359
ALCOHOL DEHYDROGENASE
KETONE/ZINGERONE SYNTHASE
4.106
12.668
80.556
112.727
83.547
30.671
9.465
34.804
3.044
99.228
3.613
36.45
7.74E-04
7.74E-04
4.18E-04
4.94E-04
3.88E-04
3.84E-04
1.29E-03
4.58E-04
8.06E-04
6.91E-04
1.14E-03
4.01E-04
4.444
2.565
1.14E-03
7.05E-04
611.736
1822.214
13706.894
262737.325
41393.53
79123.951
102324.416
40077.082
21108.132
71563.74
29043.423
29440.949
Pyrus communis
Malus x domesca
Fragaria vesca
Fragaria x ananassa
Fragaria chiloensis
Fragaria x ananassa
Prunus armeniaca
Arabidopsis thaliana
Fragaria x ananassa
Fragaria x ananassa
Solanum tuberosum
Nandina domesca
7E-34
9E-177
0.0
1E-25
3E-52
5E-98
6E-142
3E-67
0.0
7E-102
3E-87
3E-98
AY534530
AY517491
AF193790
AF193789
FJ548610
JN089766
EU395433
NM_124916
AF193791
AY048861
AB192882
FJ789568
0.0
0
HM240512
JN166691
CLUSTER UP(ABA0AUX0)
34817.814 Prunus dulcis x Prunus persica
3645.113 Rubus idaeus
Aharoni, A. 2000
Gonzlez, M. 2009
Cumplido-Laso, G. 2012
Aharoni, A. 2000
Raab, T. 2006
Putave funcon
p-value
Up regulated
a.u.i.
e-value
Reference
CLUSTER UP(ABA+AUX-)
gene26030
gene14343
gene31094
gene34867
gene06191
gene28118
gene21343
gene06193
gene15177
gene17555
gene05463
gene16186
gene21638
gene19241
gene31030
gene26403
gene13718
ALPHA-EXPANSIN 3
ANNEXIN
BETA-1,4-MANNOSYL-GLYCOPROTEIN
ENDO-BETA-1,4-GLUCANASE
ENDO-1,4-BETA-GLUCANASE
EXPANSIN
EXPANSIN 2
INVERTASE/PECTIN METHYLESTERASE INHIBITOR
MANNAN ENDO-1,4-BETA-MANNOSIDASE
PECTATE LYASE B (FAPLB)
PECTIN METHYLESTERASE
POLYGALACTURONASE
POLYGALACTURONASE 1 (FAPG1)
POLYGALACTURONASE 2 (FAPG2)
RHAMNOGALACTURONATE LYASE (FARGLYASE)
XYLOGLUCAN GLYCOSYLTRANSFERASE
XYLOGLUCAN:XYLOGLUCOSYL TRANSFERASE
gene04127
gene16326
HYDROXYPROLINE-RICH GLYCOPROTEIN
XYLOGLUCAN GALACTOSYLTRANSFERASE KATAMARI1
7.218
14.816
22.037
444.724
12.972
2.541
3.514
7.621
4.934
4.059
5.545
5.382
14.459
3.205
25.988
4.841
10.015
5.49E-04
4.16E-04
6.42E-04
3.82E-04
4.47E-04
2.96E-03
7.05E-04
1.44E-03
6.80E-04
1.11E-03
8.30E-04
1.07E-03
4.09E-04
1.45E-03
9.80E-04
1.93E-03
3.89E-04
2.847
6.428
9.78E-04
2.37E-03
1135.409
31932.04
5872.412
117102.147
101516.363
5686.578
27077.312
1576.893
44606.809
79298.451
27998.146
752.122
1905.208
15925.282
1799.52
2613.867
14733.559
3E-125
9E-180
3E-71
4E-45
0.0
2E-135
0.0
6E-76
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
2E-132
AY435101
AF188832
NM_101170
AJ414709
AF074923
AB370116
AF159563
XP_009351520
EF568778
AF339024
U25649
XM_002274102
DQ458990
AY280662
AY282613
XM_003543785
NM_102950
9E-141
1E-78
XM_002311511
XM_003617783
Bentez-Burraco, A. 2003
CLUSTER UP(ABA+AUX0)
8638.53 Populus trichocarpa
1835.538 Medicago truncatula
CLUSTER UP(ABA0AUX-)
gene05164
BETA XYLOSIDASE
gene04618
gene03446
gene22434
gene10629
gene00522
gene11447
gene31031
BETA-1,3-GLUCANASE
BETA-1,3-GLUCANASE
PECTINESTERASE
PECTINESTERASE
POLYGALACTURONASE-INHIBITING PROTEIN
PROLINE-RICH CELL WALL PROTEIN
RHAMNOGALACTURONATE LYASE PROTEIN
gene12291
gene00663
XYLOGLUCAN ENDOTRANSGLYCOSYLASE
XYLOGLUCAN ENDOTRANSGLYCOSYLASE HYDROLASE
4.05
6.44E-04
5.65
25.36
5.32
3.89
13.34
8.58
54.25
2.51E-04
3.81E-04
1.64E-03
3.07E-03
4.10E-04
6.94E-04
5.73E-04
6.00
3.78
6.12E-04
8.07E-04
Fragaria x ananassa
Ziziphus jujuba
Arabidopsis thaliana
Arabidopsis thaliana
Rubus idaeus
Vis vinifera
Arabidopsis thaliana
0.0
AY486104
0.0
0.0
7E-161
0.0
0.0
3E-04
0.0
AY170375
DQ093571
NM_115763
NM_116466
CAF04462
AJ237982
NM_127827
2E-165
3E-35
AGR44475
DQ204724
CLUSTER UP(ABA0AUX0)
gene01893
gene05671
BETA-1,3-GLUCANASE
gene12025
EXOPOLYGALACTURONASE
8.462
1.44E-04
13.436
5.73E-04
4E-118
EU676805
2.772
4.61E-03
9E-116
XM_002301453
0.0
NM_105142
Fleshy fruit development and ripening is a high complex process that includes the coordination of many metabolic pathways involved in colour, taste, firmness, flavour and turgor
required to produce a normal ripe fruit. All these process underlying fruit receptacle development and ripening must be
carefully regulated. Our microarray analysis has identified
several transcription factors (TFs) and regulatory proteins
whose expression pattern allowed its inclusion into each
ripening-related cluster (Fig. 3).
Up-regulated transcription factors
The microarray expression studies showed that 17 genes coding transcription factors belonging to Cluster UP(ABA +
AUX-) and 7 genes to Cluster UP(ABA + AUX0) (Fig. 3).
Six TFs present high level of transcripts in red ripe receptacles
(Table 6; Table S20). Genes gene31413, gene28435,
gene09407 and gene24494 code three R2R3 MYB TFs and
a MADS-box TF (FaSHP; SHATTERPROOF-like gene) respectively. FaMYB10 (gene 31413) has been described as a
indicates the total signal intensity for each feature on the microarray
platform. Gene ID in purple indicates specifity of expression in ripe
receptacle against to vegetative tissues
Putave funcon
p-value
a.u.i.
Reference
CLUSTER UP(ABA+AUX-)
gene09603
gene20939
gene04128
gene21346
gene32333
gene29482
gene29483
gene30926
gene20700
gene08569
gene14611
gene12591
gene07065
gene25577
gene25260
gene04262
gene23261
gene26353
gene18829
gene26265
gene20181
gene26249
gene24225
gene26352
gene12591
gene14947
4-COUMARATE-COA LIGASE
ANTHRANILATE SYNTHASE ALPHA SUBUNIT
ANTHRANILATE SYNTHASE BETA SUBUNIT
CHALCONE FLAVONONE ISOMERASE (CHI)
CINNAMOYL COA REDUCTASE (CCR)
CINNAMOYL COA REDUCTASE
CINNAMOYL COA REDUCTASE
CINNAMOYL-COA HYDRATASE-DEHYDROGENASE (CHD)
CINNAMYL ALCOHOL DEHYDROGENASE (CAD)
CINNAMYL ALCOHOL DEHYDROGENASE
FLAVANONE 3-HYDROXYLASE (FHT)
FLAVONOID 3-O-GLUCOSYLTRANSFERASE (FAUFGT)
FRA A 2 ALLERGEN (FRAA2)
GLUCOSYLTRANSFERASE
ISOFLAVONE REDUCTASE (EUGENOL SYNTHASE; FAEGS2)
MALONYL-COA:ISOFLAVONE 7-O-GLUCOSIDE-6''-O-MALONYLTRANSFERASE
PHENYLALANINE AMMONIA LYASE (PAL)
PHENYLPROPANOID:GLUCOSYLTRANSFERASE
POLYPHENOL OXIDASE 2 (PPO2)
UDP-GLUCOSE GLUCOSYLTRANSFERASE
UDP-GLUCOSE GLUCOSYLTRANSFERASE
UDP-GLUCOSE GLUCOSYLTRANSFERASE
UDP-GLUCOSE GLUCOSYLTRANSFERASE
UDP-GLUCOSE GLUCOSYLTRANSFERASE
UDP-GLUCOSE:CINNAMATE GLUCOSYLTRANSFERASE
UDP-RHAMNOSE:RHAMNOSYLTRANSFERASE
gene28093
gene24967
gene25258
gene25257
CINNAMATE-4-HYDROXYLASE
CINNAMYL ALCOHOL DEHYDROGENASE
ISOFLAVONE REDUCTASE
ISOFLAVONE REDUCTASE
gene15845
gene03747
gene30778
CINNAMOYL-COA REDUCTASE
FLAVONOL SYNTHASE/FLAVANONE 3-HYDROXYLASE
16.273
16.707
17.342
2.86
5.86
13.863
14.761
4.256
348.576
35.373
2.697
190.971
7.103
3.886
945.604
16.965
3.042
5.679
14.979
11.401
31.879
2.408
41.256
2.561
240.118
21.319
4.86E-04
4.22E-04
3.87E-04
1.03E-03
6.19E-04
4.57E-04
5.35E-04
1.42E-03
3.79E-04
3.90E-04
1.25E-03
8.27E-04
1.02E-03
5.82E-04
1.14E-03
1.03E-03
1.71E-03
5.08E-04
4.93E-04
4.08E-04
3.72E-04
3.06E-03
4.01E-04
1.46E-03
3.80E-04
3.77E-04
71314.032
2198.718
13939.922
219991.684
4490.154
5311.66
6119.27
40490.529
152638.488
15980.983
255100.62
34629.998
84071.637
755.83
10732.21
1048.548
57410.815
15288.679
2805.2
99900.157
1602.396
2467.037
6709.78
844.524
25063.16
3726.085
Arabidopsis thaliana
Arabidopsis thaliana
Populus trichocarpa
Prunus persica
Fragaria x ananassa
Populus trichocarpa
Populus trichocarpa
Petunia x hybrida
Fragaria x ananassa
Camellia sinensis
Fragaria x ananassa
Fragaria x ananassa
Fragaria x ananassa
Vis vinifera
Fragaria x ananassa
Glycine max
Fragaria x ananassa
Nicoana tabacum
Fragaria pentaphylla
Fragaria x ananassa
Fragaria x ananassa
Fragaria x ananassa
Fragaria x ananassa
Fragaria x ananassa
Fragaria x ananassa
Fragaria x ananassa
0.0
0.0
2E-122
9E-116
3E-106
1E-132
1E-158
0.0
0.0
4E-176
0.0
0.0
1E-102
3E-27
0.0
2E-92
0.0
1E-163
0.0
0.0
0.0
0.0
0.0
3E-165
0.0
2.00E-179
NM_116755
M92353
XM_002314725
HM543569
AY285922
XM_002314017
XM_002314016
JX142126
U63534
GQ438848
AY691918
AY695815
GQ148818
JN164680
AGV02008.1
NM_001249890
HM641823
AF346431
HM063946
AY663785
AY663786
DQ289586
DQ289587
DQ289588
AY663784
AY663787
Blanco-Portales, R. 2002
Almeida, JR. 2007
Almeida, JR. 2007
Muoz, C. 2010
Aragez, I. 2013
Pombo, MA. 2011
Lunkenbein, S. 2006
Lunkenbein, S. 2006
Griesser, M. 2008
Griesser, M. 2008
Griesser, M. 2008
Lunkenbein, S. 2006
Lunkenbein, S. 2006
CLUSTER UP(ABA+AUX0)
5.436
2.271
5.539
8.14
2.56E-04
1.36E-03
5.25E-04
9.10E-04
15892.832
11025.849
17012.885
2265.382
Rubus occidentalis
Sinopodophyllum hexandrum
Glycine max
Pyrus communis
0.0
0
1E-170
4E-109
FJ554629
HQ268590
AF202184
AF071477
CLUSTER UP(ABA0AUX-)
5.45
1.22E-03
13.45
3.058
4.06E-04
2.52E-03
gene16550
12.37
4.73E-04
gene17831
gene04258
gene09318
gene26345
ISOFLAVONE 3'-HYDROXYLASE
ISOFLAVONE 7-O-GLUCOSIDE-6''-O-MALONYLTRANSFERASE
NAD(P)H-DEPENDENT 6'-DEOXYCHALCONE SYNTHASE
PHENYLPROPANOID :GLUCOSYLTRANSFERASE
52.37
8.62
2.348
2.406
3.80E-04
6.39E-04
1.47E-03
1.80E-03
2126.824
2844.052
759.62
714.89
Medicago truncatula
Glycine max
Medicago truncatula
Nicoana tabacum
gene30434
gene00494
gene26344
gene24224
gene06602
POLYPHENOL OXIDASE
PROBABLE CINNAMYL ALCOHOL DEHYDROGENASE
UDP-GLUCOSE GLUCOSYLTRANSFERASE
UDP-GLUCOSE GLUCOSYLTRANSFERASE
59.21
20.49
2.821
451.72
3.86
9.86E-04
1.19E-03
1.75E-03
4.86E-04
7.39E-04
2318.431
2041.434
881.11
2664.134
9323.865
Potenlla frucosa
Vis vinifera
Fragaria x ananassa
Fragaria x ananassa
Malus x domesca
gene03689
gene27021
gene01708
UDP-GLUCOSE:FLAVONOID 7-O-GLUCOSYLTRANSFERASE
0.0
AY285922
5E-162
4E-126
GQ149700
XM_003609420
3E-120
XP_002273086
1E-108
3.00E-73
2E-117
2E-177
AY278228
AB291059
XM_003607060
AF346431
0.0
6E-98
0.0
0.0
0.0
DQ851214
XP_002277375
DQ289588
AY663786
AY786997
3E-165
8E-174
0
XM_003533408
XM_002530352
XM_002267629
Griesser, M. 2008
Lunkenbein, S. 2006
CLUSTER UP(ABA0AUX0)
2.569
2.154
2.153
1.11E-03
1.16E-03
8.39E-04
Putave funcon
Fold
p-value
a.u.i.
e-value
Reference
CLUSTER UP(ABA+AUX-)
gene15086
gene16428
gene32451
gene19766
gene18789
gene10626
gene14921
gene22011
gene19498
gene30534
gene14839
gene14837
gene30403
gene21537
gene03720
gene03716
1-ACYL-SN-GLYCEROL-3-PHOSPHATE ACYLTRANSFERASE
ACYL CARRIER PROTEIN
ACYL:COA LIGASE
ACYL-COA--STEROL O-ACYLTRANSFERASE
ALPHA-CARBOXYLTRANSFERASE
EPOXIDE HYDROLASE
EPOXIDE HYDROLASE
GDSL ESTERASE/LIPASE
MALONYL-COA DECARBOXYLASE FAMILY PROTEIN
NON-SPECIFIC LIPID-TRANSFER PROTEIN 2
O-ACYLTRANSFERASE WSD1
O-ACYLTRANSFERASE WSD1
SPHINGOLIPID DELTA-4 DESATURASE
STEAROYL-ACP DESATURASE
THIOESTERASE
THIOESTERASE
14.735
9.246
4.454
27.514
8.458
6.538
6.244
12.902
6.193
48.826
621.993
106.07
2.825
9.78
53.345
65.231
7.70E-04
3.89E-04
7.71E-04
5.11E-04
8.70E-04
5.23E-04
5.25E-04
9.78E-04
7.85E-04
4.45E-04
4.33E-04
2.79E-02
1.05E-03
6.32E-04
5.48E-04
3.84E-04
gene12921
gene31042
BETA-KETOACYL-ACP SYNTHASE
PHOSPHOLIPASE D
2.01
36.321
4.06E-02
4.08E-04
gene25083
gene25061
gene16355
gene08561
gene05435
gene05818
gene08996
gene13454
12-OXOPHYTODIENOATE REDUCTASE
3-OXOACYL-[ACYL-CARRIER-PROTEIN] REDUCTASE
ACYL-COENZYME A OXIDASE
GDSL ESTERASE/LIPASE
GDSL ESTERASE/LIPASE
LONG CHAIN ACYL-COA SYNTHETASE
MONOGLYCERIDE LIPASE
OMEGA-3 DESATURASE
3.111
2.028
8.64
10.38
4.28
5.24
4.59
11.66
7.21E-04
2.11E-03
4.96E-04
5.26E-04
2.06E-03
1.32E-03
6.39E-04
4.57E-04
gene06158
gene00708
gene06841
gene13295
gene15770
gene11707
4.019
5.119
2.002
2.334
2.334
2.319
4.62E-03
1.67E-03
5.01E-04
2.90E-03
9.57E-04
1.41E-03
1533.064
250709.656
12468.596
35119.281
4229.298
4240.341
1359.326
2357.557
7642.606
16848.37
1423.823
951.027
4293.257
21938.505
1117.897
1332.166
Lotus japonicus
Fragaria vesca
Populus trichocarpa
Glycine max
Jatropha curcas
Arabidopsis thaliana
Arabidopsis thaliana
Arabidopsis thaliana
Arabidopsis lyrata subsp. lyrata
Pyrus x bretschneideri
Vis vinifera
Populus trichocarpa
Arabidopsis thaliana
Vernicia montana
Vis vinifera
Arabidopsis thaliana
0.0
1E-94
0.0
2E-99
0.0
1E-155
1E-78
8E-103
2E-162
1E-25
3E-79
2E-37
0.0
0.0
3E-88
7E-64
AP004969
AJ001446
XM_002322437
XM_003534777
GQ845013
NM_116467
NM_114960
NM_102626
XM_002872641
XP_009357786
XM_002274486
XM_002328929
NM_116731
EU072353
AM447422
NM_105497
CLUSTER UP(ABA+AUX0)
715.004 Arachis hypogaea
2984.85 Cucumis savus
0.0
0.0
EU823327
EF363796
CLUSTER UP(ABA0AUX-)
2484.61
10889.97
1933.611
1459.027
3628.274
2526.885
10229.516
3907.154
Theobroma cacao
Glycine max
Arabidopsis thaliana
Arabidopsis thaliana
Arabidopsis thaliana
Vis vinifera
Cicer arienum
Prunus persica
3E-89
3E-125
0.0
6.00E-118
8E-103
0.0
0.0
EOY17386
XM_003518929
NM_125910.5
NM_202420
NM_104270
XP_002277936
XP_004501143
AF517831
5E-32
0.0
0.0
5E-41
0.0
1E-135
FJ768733
XM_002314327
NM_111566
XM_004157866
XM_002516928
XM_003619775
CLUSTER UP(ABA0AUX0)
5411.52
704.991
1749.846
3023.973
1189.399
3941.997
Arachis hypogaea
Populus trichocarpa
Arabidopsis thaliana
Cucumis savus
Ricinus communis
Medicago truncatula
Putave funcon
p-value
a.u.i.
Up regulated
CLOSER homologs in other plant species
e-value
Reference
CLUSTER UP(ABA+AUX-)
gene24494
gene07057
gene32084
gene30478
gene20865
gene25547
gene32526
gene13212
gene12519
gene29766
gene28435
gene31413
gene25060
gene28720
AGAMOUS (FASHP)
AP2 DOMAIN CLASS TRANSCRIPTION FACTOR
AP2/ERF DOMAIN-CONTAINING TRANSCRIPTION FACTOR
BASIC HELIX-LOOP-HELIX
BEL1 HOMEODOMAIN PROTEIN
C2H2L DOMAIN CLASS TRANSCRIPTION FACTOR
DOF ZINC FINGER PROTEIN
GRAS FAMILY TRANSCRIPTION FACTOR
LURP-ONE-RELATED PROTEIN (TUBBY C 2 DOMAIN CONTAINING PROTEIN)
NAC DOMAIN PROTEIN
R2R3 MYB TRANSCRIPTION FACTOR (FAEOBII)
R2R3 MYB TRANSCRIPTION FACTOR (FAMYB10)
R2R3 MYB TRANSCRIPTION FACTOR (TT2)
WRKY TRANSCRIPTION FACTOR
5.938
3.891
4.481
6.539
5.277
10.435
35.854
5.087
328.446
23.533
25.21
417.84
129.981
120.181
8.16E-04
2.31E-03
1.32E-02
3.66E-03
1.13E-03
1.44E-03
2.62E-03
5.05E-04
1.43E-03
5.20E-04
1.57E-03
3.79E-04
3.85E-04
4.48E-04
gene19478
gene01340
gene26009
gene21047
gene23830
gene02417
gene13301
gene19715
gene09407
gene30204
5907.602
4262.951
851.933
791.585
751.109
1333.306
2268.309
19090.26
924.15
3718.698
3198.538
25737.348
1398.983
11400.684
Fragaria x ananassa
Malus x domesca
Populus trichocarpa
Arabidopsis thaliana
Vis vinifera
Malus x domesca
Medicago truncatula
Fragaria x ananassa
Vis vinifera
Populus trichocarpa
Fragaria x ananassa
Fragaria x ananassa
Rosa rugosa
Medicago truncatula
10.244
2.36E-03
28.846
2.109
4.11E-04
7.51E-03
4.972
19.922
3.01
2.184
58.178
2.212
19.494
8E-177
3E-74
6E-63
4E-20
2E-80
3E-38
3E-49
2E-156
2E-77
6E-117
8E-82
1E-41
6E-46
5E-62
AGU92563.1
GU732439
XM_002304518
NM_179381
XM_002277567
HM122497
XM_003602109
XM_002305878
XM_002278173
XM_002305738
KM099230
EU155162
FR828543
XM_003617375
2E-82
GQ377448
Daminato, M. 2013
Pillet, 2015
Medina-Puche, L. 2015
Medina-Puche, L. 2014
CLUSTER UP(ABA+AUX0)
4.83E-04
1.04E-04
1.29E-03
2.47E-03
5.58E-04
1.76E-03
4.73E-04
1269.657
6757.179
2023.13
3060.134
1472.388
3987.974
729.478
Malus x domesca
Medicago truncatula
Medicago truncatula
Malus x domesca
Medicago truncatula
Fragaria chiloensis
Prunus persica
1E-45
2E-39
6E-97
1E-57
4E-52
8E-116
2E-122
GU732462
XM_003611682
XM_003601023
HM122592
XM_003601151
GQ867222
XP_007205582
Malus x domesca
Populus trichocarpa
Glycine max
Malus x domesca
Malus domesca
Rosa rugosa
Glycine max
Rosa rugosa
Humulus lupulus
Malus x domesca
Malus domesca
Malus x domesca
Malus domesca
Medicago truncatula
Arabidopsis thaliana
Medicago truncatula
Fragaria x ananassa
Solanum tuberosum
Nicoana tabacum
Medicago truncatula
4E-43
7.00E-37
1E-32
7E-179
1.00E-50
1E-118
2.00E-58
8E-153
2E-70
7E-107
1E-152
7.00E-100
5.00E-159
8E-46
7.00E-43
1E-149
3E-101
0.0
4.00E-81
1E-72
GU732450
XM_002327017
XM_003516732
HM122505
ADL36628
AFP55588
DQ822914
GU967443
FR751555
HM122664
ADL36805
HM122660
ACI13682
XM_003608713
NM_102343
XM_003590588
EU727547
AK329902
AB041520
XM_003604615
Humulus lupulus
Malus domesca
Medicago truncatula
Malus x domesca
Glycine max
Arabidopsis thaliana
7E-34
3.00E-16
1E-74
3E-54
1E-69
2E-53
FN395065
XP_008367213
XM_003590008
HM122489
XM_003556167
NM_119321
Salvaerra, A. 2013
CLUSTER UP(ABA0AUX-)
gene07304
gene04916
gene28601
gene08699
gene28452
gene12765
gene11419
gene03712
gene03865
gene07251
gene30439
gene20686
gene04424
gene32251
gene03713
gene20299
gene07210
gene03411
gene09147
gene13452
gene08033
gene11645
gene32427
gene17037
gene23226
gene01153
BASIC-LEUCINE ZIPPER
FAR1 DNA-BINDING DOMAIN CONTAINING PROTEIN
GENERAL TRANSCRIPTION FACTOR IIE SUBUNIT2
MADS-BOX TRANSCRIPTION FACTOR 22-LIKE
LOB DOMAIN-CONTAINING PROTEIN
ZINC FINGER CCCH DOMAIN-CONTAINING PROTEIN 3
7.65
48.27
3.748
2.785
5.99
11.57
8.97
4.44
3.054
2.483
5.16
19.69
5.61
25.52
74.05
2.607
11.46
417.18
6.25
7.26
5.99E-04
6.43E-04
1.38E-03
9.23E-04
5.62E-04
3.72E-04
1.72E-03
4.60E-04
1.99E-03
1.57E-03
5.59E-04
3.79E-04
8.07E-04
3.80E-04
1.74E-04
1.21E-03
4.94E-04
1.34E-03
6.02E-04
4.97E-04
1724.632
3416.356
1146.75
4424.90
1153.625
1171.102
7626.273
4321
4524.99
12917.73
1275.898
1754.341
1212.353
2950.067
1343.654
5690.84
814.522
891.421
1959.55
2184.342
Encinas-Villarejo, S. 2009
CLUSTER UP(ABA0AUX0)
3.567
3.33
2.177
3.377
3.143
2.193
3.46E-03
3.87E-02
3.39E-03
2.52E-03
1.14E-03
1.65E-03
3544.80
1749.296
2775.236
2257.018
4925.558
2161.806
Putave funcon
p-value
Up regulated
a.u.i.
e-value
CLUSTER UP(ABA+AUX-)
gene21905
gene26483
gene19112
gene26501
gene05089
gene32454
gene10659
gene02110
gene31093
gene21168
WD-REPEAT PROTEIN
28.876
4.486
447.572
9.483
2.055
5.232
12.939
4.381
6.32E-04
1.03E-03
1.10E-03
6.50E-04
2.57E-03
7.42E-04
5.40E-04
5.53E-04
5.865
6.79E-04
12.423
1.98E-03
1952.712
11234.476
22676.928
840.288
19185.487
26361.513
1087.751
7385.48
Populus trichocarpa
Arabidopsis thaliana
Oryza sava
Medicago truncatula
Phaseolus vulgaris
Vis vinifera
Glycine max
Malus domesca
0.0
1E-20
1E-25
1E-54
3E-50
0.0
4E-94
4E-127
XM_002308869
BK001754
AF090698
XM_003616359
AF145386
XM_002271554
XM_003517865
XP_008337431
0.0
0.0
XP_006358293
XP_008376375
Vis vinifera
Medicago truncatula
Arabidopsis thaliana
Arabidopsis thaliana
Arabidopsis thaliana
Medicago truncatula
Arabidopsis thaliana
Vis vinifera
Glycine max
Arabidopsis thaliana
Medicago truncatula
0.0
1E-160
0.0
2E-106
0.0
0.0
0.0
1E-148
0.0
3E-117
4E-63
XM_002272301
XM_003601211
NM_111649
NM_128240
NM_105452
XM_003608235
NM_180212
XM_002272976
XM_003549582
NM_113431.5
XM_003609219
Glycine max
Vis vinifera
Vis vinifera
Arabidopsis thaliana
3E-126
5E-69
1E-146
0.0
FJ014728
XM_003633734
XM_003633996
AF084035
KINASES
gene23258
gene06226
gene15532
gene31007
gene22182
gene30640
gene13564
gene20321
gene32170
gene17422
gene30997
ADENOSINE KINASE
PANTOTHENATE KINASE
PROTEIN KINASE DOMAIN-CONTAINING PROTEIN
PROTEIN KINASE-LIKE PROTEIN
SENSOR KINASE (CSK)
SERINE/THREONINE PROTEIN KINASE
SERINE/THREONINE PROTEIN KINASE
SERINE/THREONINE-PROTEIN KINASE
SERINE/THREONINE-PROTEIN KINASE HT1-LIKE
SERINE/THREONINE-PROTEIN KINASE OXI1 (AGC2-1)
ZINC FINGER SER/THR PROTEIN KINASE
gene05293
gene24830
gene23598
gene30661
gene10081
gene09579
gene09873
gene22281
gene00322
gene08799
gene30404
gene27006
gene18503
gene18505
gene31679
gene30186
gene16196
gene09729
gene19113
C2 DOMAIN-CONTAINING PROTEIN
C2 DOMAIN-CONTAINING PROTEIN
6.06
20.752
15.196
6.442
6.727
3.744
6.936
7.196
3.014
11.071
23.606
4.76E-04
3.78E-04
4.57E-04
5.13E-04
6.84E-04
6.19E-04
6.15E-04
4.83E-04
1.02E-03
4.55E-04
3.68E-04
13527.151
45073.96
6490.259
1227.64
14678.543
2730.391
1928.308
2113.035
5739.779
3531.296
5345.349
RECEPTORS
23.737
148.678
10.254
5.199
4.07E-04
0.00197
4.42E-03
7.36E-04
10812.41
1418.95
821.599
622.054
1.21E-03
1.80E-03
1.88E-03
3.83E-04
5.88E-03
1.48E-03
7.27E-04
5.26E-04
1.40E-03
4.04E-04
5.18E-04
8.42E-04
1.48E-03
2713.808
2149.05
1065.77
2504.649
735.698
23217.95
2100.81
9615.67
28553.73
16857.907
3251.957
1708.866
1616.508
Arabidopsis thaliana
Prunus mume
Populus trichocarpa
Pyrus pyrifolia
Medicago truncatula
Cucumis melo
Medicago truncatula
Medicago truncatula
Hevea brasiliensis
Medicago truncatula
Artemisia annua
Arabidopsis thaliana
Medicago truncatula
2E-62
NM_125180
0.0
XP_008239171
4E-53
XM_002307964
9E-08
AB545982
4E-88
XM_003589259
2E-111 XP_008445030
2E-73
XM_003637350
8E-23
XM_003590265
1E-30
HM640272
3E-08
XM_003616811
5E-11
GQ901904
3E-151
NM_201828
4E-63
XM_003602578
CLUSTER UP(ABA+AUX0)
2.801
16.454
2.10E-03
1.44E-03
0.0
4E-26
XM_006376379
NM_001054079
0
6E-10
0.0
2E-122
NM_124535
NM_001202566
XM_003555999
NM_112761
0
2E-23
4E-09
XM_002301353
AB545981
NM_118773
7E-63
1E-179
NM_001157389
XP_008219186
KINASES
gene13428
gene19366
gene20400
gene01144
2.205
2.334
3.584
4.032
gene18983
gene02131
gene04008
7.323
2.113
3.899
gene05774
gene26891
RHODOPSIN-LIKE RECEPTOR
ODORANT RECEPTOR DOMAIN CONTAINING PROTEIN(ODR-4 HOMOLOG)
2.367
4.504
7.23E-03
2.47E-03
2.03E-03
1.90E-03
732.812
1673.079
2726.689
1051.895
Arabidopsis thaliana
Arabidopsis thaliana
Glycine max
Arabidopsis thaliana
RECEPTORS
1.22E-03
8.65E-03
CLUSTER UP(ABA0AUX-)
gene09629
gene13280
gene21177
gene07367
gene18826
gene20494
gene07026
gene05178
gene20299
8.20
5.65
4.70
2.902
11.14
3.95
6.48
14.57
2.607
5.25E-04
1.03E-03
5.19E-04
3.53E-03
2.10E-04
7.62E-04
4.08E-04
4.32E-04
1.21E-03
gene15486
gene05792
gene16298
gene00913
gene16699
gene16513
gene17121
gene11097
gene11098
gene09806
gene15891
gene19993
gene29765
gene34758
gene30692
27.37
8.68
2.143
2.049
3.769
5.75
7.98
18.19
4.66
5.21
10.73
26.60
3.442
10.66
4.21
3.79E-04
4.08E-04
1.47E-03
4.14E-03
1.37E-03
9.56E-04
5.77E-04
6.97E-04
6.44E-04
9.01E-04
4.17E-04
5.69E-04
1.34E-03
1.34E-04
1.32E-03
gene03647
gene09853
gene16754
gene01188
gene16752
gene03306
gene10171
gene12032
gene32106
gene31702
gene03637
gene19216
gene23984
E3 UBIQUITIN-PROTEIN LIGASE
F-BOX FAMILY PROTEIN
F-BOX FAMILY PROTEIN
F-BOX PROTEIN
F-BOX PROTEIN
POLYUBIQUITIN
RING-H2 FINGER PROTEIN
RING-H2 FINGER PROTEIN
RING-H2 FINGER PROTEIN
RING-H2 FINGER PROTEIN
RING-H2 FINGER PROTEIN
UBIQUITIN
UBIQUITIN
gene13148
gene19496
gene30199
1001.321
1229.809
1163.741
1434.00
3704.822
3314.72
9900.003
2361.17
5690.84
Arabidopsis thaliana
Ricinus communis
Arabidopsis lyrata
Nicoana plumbaginifolia
Glycine max
Arabidopsis thaliana
Arabidopsis thaliana
Prunus mume
Medicago truncatula
6E-126
1E-45
2E-151
1E-175
1E-21
9E-164
3E-135
0.0
NM_129264
XP_002510796
XM_002864690
FJ882981
XM_003554411
NM_130366
NM_102297
XP_8223286
1E-149
XM_003590588
3214.94
1602.459
2370.38
1189.11
825.39
2221.244
1021.565
1113.888
2495.939
726.609
1052.508
6716.811
3815.13
3351.558
1892.259
Nicoana tabacum
Populus trichocarpa
Arabidopsis lyrata
Arabidopsis lyrata
Ricinus communis
Theobroma cacao
Populus nigra
Arabidopsis thaliana
Glycine max
Arabidopsis thaliana
Medicago truncatula
Theobroma cacao
Glycine max
Ricinus communis
Vis vinifera
5E-158
1E-120
0.0
2E-76
2E-26
0.0
0.0
1E-71
1E-94
0.0
0.0
4E-72
4E-135
1E-60
0.0
AY220481
DQ997692
XM_002873402
XM_002883451
XP_002513567
EOY11134
AB030083
NM_116919
XM_003544724
NM_001202923
XM_003604077
EOY02771
XR_137280
XM_002515360
XP_002270943
2E-47
3E-40
3E-70
4E-167
1E-83
0.0
2E-143
2E-144
9E-75
1E-34
8E-32
1E-21
0.0
XP_002283507
XM_002307964
XM_002308681
NM_104435
XP_004304799
L05361
XP_008219359
XP_ 008219359
XP_007210150
XM_003601970
XM_002892803
U84967
XM_003616928
0.0
0.0
0.0
XM_003555349
XM_003547220
XM_003629955
KINASES
1.51E-03
2.52E-03
2.35E-03
9.90E-04
2.37E-03
3.28E-03
1.25E-03
4.73E-04
4.01E-04
1.19E-03
6.88E-04
4.17E-04
2.31E-03
2827.567
1223.653
2953.936
1194.41
1203.989
4193.87
3108.40
868.89
1200.18
10416.78
1426.00
10609.485
1545.215
Vis vinifera
Populus trichocarpa
Populus trichocarpa
Arabidopsis thaliana
Solanum lycopersicum
Arabidopsis thaliana
Prunus mume
Prunus persica
Prunus persica
Medicago truncatula
Arabidopsis lyrata
Arabidopsis thaliana
Medicago truncatula
RECEPTORS
11.27
3.615
84.48
1.83E-04
5.31E-04
3.83E-04
Reference
(continued)
Signalling and Regulatory Proteins
GENES
Putave funcon
p-value
Up regulated
a.u.i.
e-value
Reference
CLUSTER UP(ABA0AUX0)
gene28810
gene04419
gene13353
gene31011
gene24536
gene20449
gene12722
gene11610
gene32677
gene10002
gene28410
gene13840
gene23602
gene11741
gene08498
gene05851
BON1-ASSOCIATED PROTEIN
C2 DOMAIN-CONTAINING FAMILY PROTEIN
C2 DOMAIN-CONTAINING FAMILY PROTEIN
CALMODULIN PROTEIN
CYCLIN
FLOWERING TIME CONTROL PROTEIN FY (WD40 DOMAIN CONTAINING PROTEIN)
PLECKSTRIN HOMOLOGY DOMAIN-CONTAINING FAMILY PROTEIN
PROTEIN PHOSPHATASE 2C
PROTEIN PHOSPHATASE 2C
SPX DOMAIN-CONTAINING PROTEIN
SYNTAXIN
SYNTAXIN
SYNTAXIN
SYNTAXIN
TRANSDUCIN
TRANSDUCIN
3.035
3.401
3.389
3.355
3.073
4.63
2.328
2.302
2.302
2.226
2.195
2.198
2.196
2.287
2.168
3.031
9.25E-04
1.35E-03
1.67E-03
1.51E-03
2.17E-03
1.86E-02
1.48E-03
1.41E-03
2.61E-03
1.14E-03
8.07E-04
1.20E-03
1.07E-03
4.76E-03
7.33E-03
1.29E-03
gene24690
gene14737
gene04334
gene23153
gene20924
DEPHOSPHO-COA KINASE
DEPHOSPHO-COA KINASE
DEPHOSPHO-COA KINASE
PROTEIN KINASE AND PP2C-LIKE DOMAIN-CONTAINING PROTEIN
SERINE/THREONINE/TYROSINE KINASE
2.994
2.986
2.978
2.306
2.234
2.35E-03
3.00E-03
3.05E-03
1.15E-03
2.63E-03
gene00483
gene09018
gene14751
gene17739
gene09190
gene14115
gene11337
gene15211
gene30954
gene21896
gene01044
gene02007
gene15931
gene24708
gene32136
gene23698
gene24090
gene11179
gene24698
gene14941
E3 UBIQUITIN-PROTEIN LIGASE
E3 UBIQUITIN-PROTEIN LIGASE
E3 UBIQUITIN-PROTEIN LIGASE
E3 UBIQUITIN-PROTEIN LIGASE
E3 UBIQUITIN-PROTEIN LIGASE
E3 UBIQUITIN-PROTEIN LIGASE
EID1-LIKE F-BOX PROTEIN
F-BOX PROTEIN FAMILY
F-BOX PROTEIN
F-BOX/RNI PROTEIN
F-BOX/LRR-REPEAT PROTEIN
FRATAXIN, MITOCHONDRIAL PRECURSOR
PRLI-INTERACTING FACTOR
PROTEASOME ACTIVATING PROTEIN
RING FINGER PROTEIN
UBIQUITIN CARRIER PROTEIN
UBIQUITIN EXTENSION PROTEIN
UBIQUITIN FAMILY PROTEIN
UBIQUITIN-CONJUGATING ENZYME FAMILY PROTEIN
UBIQUITIN-SPECIFIC PROTEASE
2.857
2.847
2.845
3.281
2.843
3.566
2.808
2.743
2.703
2.696
2.299
2.255
2.321
2.317
2.182
2.159
2.159
2.158
2.158
2.157
gene03054
4.444
1905.616
1347.888
955.542
1639.9
1841.267
828.33
7192.243
8840.02
1119.714
1242.786
775.611
1485.318
829.392
1129.414
994.454
3352.222
Solanum tuberosum
Populus trichocarpa
Populus trichocarpa
Medicago truncatula
Medicago truncatula
Malus domesca
Populus trichocarpa
Hevea brasiliensis
Glycine max
Vis vinifera
Ricinus communis
Populus trichocarpa
Populus trichocarpa
Glycine max
Populus trichocarpa
Arabidopsis lyrata
1E-32
0.0
0.0
1E-42
5E-111
2E-93
0.0
1E-155
2E-171
1E-126
5E-82
2E-115
2E-138
1E-111
1E-170
0.0
XM_006339390
XM_002311329
XM_006376379
XM_003602046
XM_003622816
XP_008375316
XM_002302098
EU827608
XM_003530462
XM_002283854
XM_002521518
XM_002316191
XM_002316205
NM_001254606
XM_002321649
XM_002892822
1764.206
1562.265
3340.466
870.929
7494.025
Arabidopsis thaliana
Medicago truncatula
Medicago truncatula
Medicago truncatula
Populus trichocarpa
7E-26
6E-102
8E-100
0.0
2E-51
NM_179771
XM_003593562
XM_003625853
XM_003590198
XM_006382154
0.0
3E-127
0.0
1E-123
0.0
0.0
2E-122
2E-30
3E-65
5E-174
4E-18
2E-83
5E-94
0.0
8E-18
2E-87
2E-74
0.0
8E-101
0.0
NM_001282242
XM_003615287
XM_003618721
XM_003539490
NM_120366
XP_008223431
XM_002276292
XM_002871233
XM_003624710
NM_100954
NM_117470
XP_008230187
NM_121997
NM_112178
XP_007200789
XM_003608898
XM_002322782
XM_002309840
XM_002309518
XM_002300134
0.0
XP_009376146
KINASES
785.12
960.926
1659.639
3346.186
1102.593
3354.01
2500.017
964.801
815.817
1077.042
746.853
1081.93
806.102
7671.219
815.39
4186.952
73022.762
1394.006
15916.151
745.522
Glycine max
Medicago truncatula
Medicago truncatula
Glycine max
Arabidopsis thaliana
Prunus mume
Vis vinifera
Arabidopsis lyrata subsp. lyrata
Medicago truncatula
Arabidopsis thaliana
Arabidopsis thaliana
Prunus mume
Arabidopsis thaliana
Arabidopsis thaliana
Prunus persica
Medicago truncatula
Populus trichocarpa
Populus trichocarpa
Populus trichocarpa
Populus trichocarpa
RECEPTORS
1.14E-03
Hormonal-related genes
GENES
Putave funcon
Up regulated
p-value
a.u.i.
e-value
Reference
CLUSTER UP(ABA+AUX-)
AUXINS
gene13601
gene22252
gene28375
gene08921
gene08336
gene15614
gene14862
3.994
17.972
12.131
4.152
2.487
2.799
4.24
6.03E-04
7.54E-04
2.02E-03
1.18E-03
2.01E-03
1.40E-03
1.36E-03
gene11424
gene11421
gene30779
1-AMINOCYCLOPROPANE-1-CARBOXYLATE OXIDASE
1-AMINOCYCLOPROPANE-1-CARBOXYLATE OXIDASE
ETHYLENE-FORMING-ENZYME DIOXYGENASE
27.618
29.837
39.987
1.14E-03
3.83E-04
3.77E-04
gene31337
gene18930
GA2-OXIDASE
GIBBERELLIN 20 OXIDASE
14.226
6.589
4.67E-04
5.47E-04
1085.289
40122.49
1721.586
17740.012
3174.778
3235.846
3559.66
Populus trichocarpa
Glycine max
Glycine max
Glycine max
Glycine max
Populus trichocarpa
Populus trichocarpa
0.0
0.0
5E-122
1E-158
2E-63
1E-90
4E-45
XM_002323654
XM_003531870
XM_003530787
XM_003525807
XM_003541323
XM_002308417
XM_002310820
8E-159
1E-157
5.00E-86
XM_002514098
NM_127517
U97530
4E-161
1E-95
JF441168
XM_002284938
0.0
0.0
0.0
1E-168
0.0
3E-95
0.0
3E-87
3E-98
EF580921
ADU85829.1
KC967656
GQ338153
JX848734
JN941557
FJ784889
AB192882
FJ789568
7E-94
5E-120
XM_002893011
XM_002281543
ETHYLENE
GIBBERELLINS
7839.832 Pyrus communis
5183.161 Vis vinifera
3-HYDROXY-3-METHYLGLUTARYL-COA REDUCTASE
9-CIS-EPOXYCAROTENOID DIOXYGENASE (FANCED1)
BETA-CAROTENE HYDROXYLASE
LINALOOL SYNTHASE
LINALOOL SYNTHASE (LIS)
NEOXANTHIN SYNTHASE (NSY)
PHYTOENE SYNTHASE PROTEIN
SHORT CHAIN DEHYDROGENASE
SHORT CHAIN DEHYDROGENASE/REDUCTASE
gene04119
gene15184
3.45
3.322
3.33
10.453
11.549
4.345
8.001
3.613
36.45
1.61E-03
2.62E-03
8.10E-04
3.79E-04
5.49E-04
5.37E-04
6.45E-04
1.14E-03
4.01E-04
107.15
203.162
3.73E-04
1.69E-03
8679.84
6688.363
3261.147
7798.971
45913.4
4320.998
17310.031
29043.42
29440.95
Malus x domesca
Fragaria x ananassa
Fragaria x ananassa
Acnidia arguta
Malus x domesca
Malus x domesca
Fragaria x ananassa
Solanum tuberosum
Nandina domesca
JASMONIC ACID
1193.469 Arabidopsis lyrata
40959.424 Vis vinifera
CLUSTER UP(ABA+AUX0)
gene28201
CYTOKININ-O-GLUCOSYLTRANSFERASE
gene23887
gene23886
MYRCENE SYNTHASE
TERPENE SYNTHASE
4.418
4.446
2.856
1.75E-03
gene12478
gene15204
gene05631
12-OXOPHYTODIENOATE REDUCTASE
CYTOKININ OXIDASE
GERMIN-LIKE PROTEIN
4.02
6.70
50.61
gene34980
AUXIN-INDUCED PROTEIN
2.874
8.50E-04
gene03935
gene12763
4.21
3.337
1.11E-03
3.76E-03
2E-152
XM_003615784
8E-53
2E-140
NM_001281080
JF449453
0.0
0.0
1.00E-75
NM_001246944
XM_002307645
EU116342
5E-152
XM_003626384
4E-89
2E-31
XP_008354757
XP_008376800
CLUSTER UP(ABA0AUX-)
5.40E-04
1.85E-03
5.66E-04
AUXINS
6.19
217.62
3.146
3.66E-04
9.98E-04
1.84E-03
gene01502
gene05020
GIBBERELLIN 2-OXIDASE
6.34
1.04E-03
543.34
1.79E-03
gene32005
gene15694
gene17480
1-AMINOCYCLOPROPANE-1-CARBOXYLATE OXIDASE
1-AMINOCYCLOPROPANE-1-CARBOXYLATE OXIDASE
ETHYLENE-RESPONSIVE TRANSCRIPTION FACTOR
14.363
14.239
2.802
2.27E-03
1.02E-02
1.61E-02
gene08518
4.349
8.95E-04
0.0
0.0
0.0
0.0
DQ473433
AB055512
AB294695
GQ401664
GIBBERELLINS
1766.437 Populus trichocarpa
3E-127
XM_002301494
0.0
4E-86
8E-59
AY706156
AJ890087
XM_003610878
CLUSTER UP(ABA0AUX0)
ETHYLENE
21539.965 Fragaria x ananassa
1129.594 Prunus domesca
5047.316 Medicago truncatula
GIBBERELLINS
7501.51 Fragaria x ananassa
2E-47
AF039183
3E-159
XM_006347691
XP_008230162
PERAKINE REDUCTASE
TERPENE SYNTHASE DOMAIN
2.358
3.106
1.50E-03
2.71E-03
0.0
Medina-Escobar. 1997
been questioned supporting the proposal that the early 13hydroxylation pathway that produces GA1 is really the key
pathway that renders bioactive GAs in strawberry fruits
(Symons et al. 2012). In this report, only detectable levels of
GA1 were observed while other bioactive GAs as GA3 and
GA4 were found below detection limits. Additionally, a sharp
decrease of both IAA and GA1 levels along fruit ripening was
detected (Symons et al. 2012). These studies suggest that gibberellins could play a dual regulatory role, promoting first the
growth of receptacles in combination with auxins, and a relevant role in the ripening afterwards. Our microarray studies
have shown the induction of two biosynthetic GA genes belonging to Cluster UP(ABA + AUX-) in ripe receptacles.
These genes appear to encode a GA2-oxidase (gene31337),
a catabolic enzyme that inactivates bioactive gibberellins, and
a GA20-oxidase (gene18930), a regulatory enzyme involved
in the gibberellin biosynthesis. Both genes are transcribed at
high levels only in mature receptacles, when ABA levels in
the fruit receptacle are very high (Table 8; Table S22) on the
contrary to the GA20-oxidase gene described by Chen et al.
(2015), whose expression in harvested strawberry fruit is
slightly up-regulated for exogenous IAA but repressed for
exogenous ABA. An increase in the expression of FaGA2ox
along strawberry fruit ripening was previously reported
(Csukasi et al. 2011). Gibberellin homeostasis is maintained
by a balance between their rates of biosynthesis and deactivation. Thus, our results are partially contradictory with those
reported previously (Csukasi et al. 2011), as far as an upregulation of a regulatory gibberellin biosynthetic gene along
the receptacle ripening process was observed. Thus, our microarray study does not support an important role for GAs on
the ripening process.
Transporters
A large number of genes induced in ripen receptacle encode
proteins involved in transport processes (Fig. 3). For instance,
several genes corresponding to ATP-binding cassette (ABC)
and multi-antimicrobial extrusion protein (MATE) transporters are components of Clusters UP(ABA + AUX-),
UP(ABA0AUX-) and UP(ABA0AUX0). Glutathione Stransferases (GSTs) are also included in these three clusters
(Table 9; Table S23).
Two major transport systems have been described in the
tonoplast membrane. The primary transport system is mediated
by ABC transporters, while a secondary transport mechanism is based on the pre-existence of a H+ gradient across
the vacuolar membrane produced by V-, P-ATPases or
vacuolar H + pyrophosphatase (Martinoia et al. 2007;
Verweij et al. 2008).
Several reports have shown that different flavonoids and
phenylpropanoids, as acylated anthocyanin, are transported
inside the vacuole through MATE transporters (Gomez et al.
Putave funcon
Up
regulated
Fold
p-value
a.u.i.
e-value
Reference
CLUSTER UP(ABA+AUX-)
gene00123
gene22891
gene30234
gene21322
gene01994
gene10386
gene09427
gene10387
gene10383
gene31672
gene09426
gene18167
gene07028
gene20514
gene01912
gene30855
gene26473
ABC TRANSPORTER
ABC TRANSPORTER
ABC TRANSPORTER
ADENINE/GUANINE PERMEASE
EQUILIBRATIVE NUCLEOTIDE TRANSPORTER 3
GLUTATHIONE S-TRANSFERASE
GLUTATHIONE S-TRANSFERASE
GLUTATHIONE S-TRANSFERASE
GLUTATHIONE S-TRANSFERASE
GLUTATHIONE S-TRANSFERASE
GLUTATHIONE S-TRANSFERASE
GLUTATHIONE-S-TRANSFERASE
MATE EFFLUX DOMAIN-CONTAINING PROTEIN
OLIGOPEPTIDE TRANSPORTER OPT FAMILY
OLIGOPEPTIDE TRANSPORTER OPT FAMILY
SUGAR TRANSPORT PROTEIN
TAMBA BLACK MULTIDRUG RESISTANCE PUMP
7.58
10.379
34.236
7.178
8.871
6.61
698.211
9.558
5.496
1215.977
68.032
19.889
56.292
3.252
2.807
5.445
11.881
4.24E-04
4.10E-04
3.64E-04
5.84E-04
6.25E-04
4.86E-04
1.44E-03
1.02E-03
6.03E-04
8.36E-04
5.91E-04
3.77E-04
4.04E-04
2.51E-03
2.26E-03
4.94E-04
8.29E-04
gene00122
gene08245
gene00933
gene13437
9.636
2.114
2.231
2.931
5.87E-04
4.60E-03
1.28E-03
1.34E-03
gene08088
gene08792
3.618
2.347
3.71E-03
2.20E-03
gene25969
gene04460
gene23188
gene19956
gene06067
gene28763
gene21219
gene09638
gene11065
gene15073
gene03636
gene03634
gene18485
gene11300
gene06443
gene27784
gene14598
gene18781
gene08357
gene10072
gene15923
gene05814
gene12037
ABC TRANSPORTER
AMINO ACID TRANSPORTER
ANION-TRANSPORTING ATPASE FAMILY PROTEIN
CATIONIC AMINO ACID TRANSPORTER
CYCLIC NUCLEOTIDE-GATED ION CHANNEL
GLUTATHIONE S-TRANSFERASE
GLYCEROL-3-PHOSPHATE TRANSPORTER
IMPORTIN
IMPORTIN
MATE EFFLUX FAMILY PROTEIN
MATE EFFLUX FAMILY PROTEIN
MATE EFFLUX FAMILY PROTEIN
METAL TOLERANCE PROTEIN
MITOCHONDRIAL INNER MEMBRANE TRANSLOCASE
MITOCHONDRIAL PHOSPHATE TRANSPORTER
MITOCHONDRIAL SUBSTRATE CARRIER FAMILY PROTEIN
OLIGOPEPTIDE TRANSPORTER
ORGANIC ANION TRANSPORTER
PLEIOTROPIC DRUG RESISTANCE PROTEIN
POTASSIUM CHANNEL TETRAMERIZATION DOMAIN-CONTAINING PROTEIN
SOLUTE CARRIER
SUGAR TRANSPORTER
TRANSPARENT TESTA 12
gene23477
gene02466
gene28000
gene10994
gene24391
gene24391
gene11125
gene01202
gene08766
gene12262
gene13420
gene24796
gene06384
gene17615
gene12355
gene01833
gene18545
gene01868
gene06304
gene18771
gene31711
gene16819
ABC TRANSPORTER
ABC TRANSPORTER A FAMILY MEMBER 1
AMINO ACID TRANSPORTER
CATION/H(+) ANTIPORTER
COPPER TRANSPORTER
COPPER TRANSPORTER
CRCB PROTEIN
GLUTATHIONE S-TRANSFERASE
GLUTATHIONE S-TRANSFERASE
GLUTATHIONE-S-TRANSFERASE
MAGNESIUM TRANSPORTER
MALTOSE TRANSPORTER
METAL TRANSPORTER
NUCLEOPROTEIN TPR
PEROXISOMAL MEMBRANE ABC TRANSPORTER FAMILY
RAE1 PROTEIN
RAE1 PROTEIN
SOLUTE CARRIER FAMILY
SUCROSE TRANSPORTER
TRANSLOCON AT THE OUTER MEMBRANE OF CHLOROPLASTS
VACUOLAR AMINO ACID TRANSPORTER
VACUOLAR ATP SYNTHASE SUBUNIT F
1788.617
1055.205
4836.517
739.272
919.54
77511.06
21314.41
5451.908
137548.723
10454.536
4297.895
45008.625
6939.15
1537.641
2260.423
5442.932
735.659
Vis vinifera
Nicoana tabacum
Vis vinifera
Arabidopsis thaliana
Prunus mume
Glycine max
Glycine max
Cicer arienum
Carica papaya
Malus x domesca
Lycopersicon esculentum
Rheum australe
Arabidopsis thaliana
Medicago truncatula
Populus trichocarpa
Arabidopsis thaliana
Glycine max
1E-165
0.0
2E-133
0.0
0.0
7E-62
6E-82
4E-99
1E-113
3E-115
7E-79
2E-114
1E-40
0.0
0.0
0.0
2E-162
XM_002281034
AJ831379
XM_002277136
NM_111933
XP_008230198
NM_001250784
NM_001248057
XM_004488650
AJ000923
JN573600
AY007561
EU931209
NM_124290
XM_003625124
XM_002303648
NM_116436.5
JN316209
Populus trichocarpa
Glycine max
Arabidopsis thaliana
Populus trichocarpa
0
6E-47
3E-115
2E-68
XM_006383944
XP_003523404
NM_101997
XM_002308250
4E-169
6E-142
XM_002307607
NM_179737
Arabidopsis thaliana
Populus trichocarpa
Arabidopsis lyrata
Populus trichocarpa
Arabidopsis thaliana
Pyrus communis
Glycine max
Arabidopsis thalian
Glycine max
Arabidopsis thaliana
Arabidopsis lyrata
Vis vinifera
Glycine max
Arabidopsis thaliana
Zea mays
Arabidopsis thaliana
Populus trichocarpa
Arabidopsis lyrata
Populus trichocarpa
Arabidopsis lyrata
Medicago truncatula
Ricinus communis
Pyrus x bretschneideri
0.0
7E-171
0.0
0.0
3E-45
3E-123
0.0
0.0
0.0
0.0
2E-91
0.0
0.0
2E-69
2E-160
1E-77
0.0
9E-159
3E-91
0.0
0.0
0E+00
0.0
NM_114646
XM_002323825
XM_002882617
XM_002303678
NM_124692
DQ901400
XM_003534317
NM_120385
XM_003532937
NM_103646
XM_002890044
XP_002280212
XP_003532918
AY463970
NM_001111372
NM_148200.5
XM_002303648
XM_002884794
XM_002298087
XM_002878690
XM_003596504
XP_002517216
XP_009373462
Arabidopsis thaliana
Prunus mume
Populus trichocarpa
Solanum lycopersicum
Vis vinifera
Vis vinifera
Medicago truncatula
Vis vinifera
Vis vinifera
Ricinus communis
Vis vinifera
Malus x domesca
Medicago truncatula
Ricinus communis
Theobroma cacao
Arabidopsis thaliana
Glycine max
Vis vinifera
Fragaria x ananassa
Arabidopsis thaliana
Vis vinifera
Zea mays
0.0
0.0
7E-173
0
1E-39
1E-39
1E-117
4E-102
1E-70
7E-114
5E-43
8E-171
1E-25
0.0
0.0
0.0
2E-155
5E-179
3E-05
0.0
3E-148
9E-71
NM_001204044
XP_008244242
XM_002311042
XM_004245503
HQ108189
HQ108189
XM_003601034
XM_002263350
XM_002275399
XM_002525018
XM_002282109
DQ648082
XM_003608272
XM_002518775
XM_007047913
NM_106715
NM_001255101
XM_002271889
JX013937
NM_112678
XM_002270872
NM_001156371
CLUSTER UP(ABA+AUX0)
6973.567
4009.868
17114.828
3372.606
CLUSTER UP(ABA0AUX-)
8.52
11.36
3.105
31.32
20.58
13.18
3.432
2.698
3.093
12.18
8.41
41.62
6.48
4.46
4.82
6.79
7.43
2.802
9.61
2.861
37.09
6.87
13.72
4.64E-04
5.08E-04
2.58E-03
6.09E-04
1.57E-04
1.04E-03
1.01E-03
4.24E-03
8.26E-04
3.85E-04
5.19E-03
2.05E-03
1.01E-03
3.95E-02
8.58E-04
7.55E-04
4.25E-04
1.94E-03
4.40E-04
1.08E-03
3.82E-04
6.18E-04
3.82E-04
1994.979
4799.353
1144.99
1231.89
1195.681
3014.172
7107.59
910.19
2640.33
3120.928
2051.198
808.352
6562.629
1904.287
746.01
1874.232
1786.545
1423.83
1072.145
929.08
12576.247
1700.711
1327.47
CLUSTER UP(ABA0AUX0)
5.175
2.524
4.427
3.342
4.253
4.253
3.352
2.656
2.654
2.649
2.535
2.532
2.525
2.372
2.001
9.954
56.546
2.228
2.212
2.167
2.025
2.022
5.73E-03
1.53E-03
1.65E-03
6.15E-04
1.84E-02
1.84E-02
5.75E-04
1.50E-03
4.75E-04
1.09E-03
4.86E-04
2.01E-03
2.58E-03
1.05E-03
1.13E-03
2.83E-04
1.46E-03
2.52E-03
8.77E-04
2.36E-02
5.72E-04
1.60E-03
1454.141
1072.99
3619.209
1139.307
998.343
998.343
2246.614
5403.135
11405.731
5785.333
911.56
1869.195
1542.737
1113.076
3820.646
3031.32
4379.698
1747.197
1347.417
920.235
6382.371
8532.878
Jia, H. 2013
Putave funcon
(a.u.i.) indicates the total signal intensity for each feature on the
microarray platform. Gene ID in purple indicates specifity of expression
in ripe receptacle against to vegetative tissues
p-value
Up regulated
a.u.i.
e-value
Reference
CLUSTER UP(ABA+AUX-)
PRIMARY METABOLISM
gene04580
gene05994
gene26175
gene25718
gene22813
gene13140
6-PHOSPHOGLUCONOLACTONASE
D-GLYCERATE 3-KINASE
ENOLASE
HEXOKINASE
PYRUVATE DEHYDROGENASE
PYRUVATE KINASE
gene27452
gene09899
gene16498
gene01062
gene23979
gene31924
gene03646
gene23438
gene19242
gene18910
gene29713
gene21929
gene26121
gene00616
gene16551
gene22147
gene19737
gene01893
gene08027
gene12578
gene22433
gene11229
gene20643
gene28508
gene22484
gene03985
gene16488
gene28822
gene07324
gene07016
gene34199
gene27856
gene05154
gene17835
gene17836
gene09927
gene32455
gene08940
gene32694
gene24141
gene31205
gene30876
gene11912
gene27838
gene16656
gene28414
gene12969
gene10008
gene21507
gene21033
gene30707
gene14267
gene09003
gene02228
gene11108
gene08702
gene12064
gene00649
2-NITROPROPANE DIOXYGENASE
2-NITROPROPANE DIOXYGENASE
2-OXOGLUTARATE (2OG) AND FE(II)-DEPENDENT OXYGENASE
2-OXOGLUTARATE (2OG) AND FE(II)-DEPENDENT OXYGENASE
2-OXOGLUTARATE (2OG) AND FE(II)-DEPENDENT OXYGENASE
2-OXOGLUTARATE (2OG) AND FE(II)-DEPENDENT OXYGENASE
2-OXOGLUTARATE (2OG) AND FE(II)-DEPENDENT OXYGENASE
3-HYDROXYISOBUTYRYL-COA HYDROLASE
3-HYDROXYISOBUTYRYL-COA HYDROLASE
3-HYDROXYISOBUTYRYL-COA HYDROLASE
ACETOLACTATE SYNTHASE SMALL SUBUNIT
ACETOLACTATE SYNTHASE SMALL SUBUNIT
ADENINE NUCLEOTIDE ALPHA HYDROLASES
ALDO-KETO REDUCTASE
ALDO-KETO REDUCTASE
ALDO-KETO REDUCTASE
ALTERNATIVE OXIDASE 4
AMINOACRYLATE HYDROLASE
ANKYRIN REPEAT DOMAIN-CONTAINING PROTEIN
ATPASE FAMILY AAA DOMAIN-CONTAINING PROTEIN
ATP-DEPENDENT DNA HELICASE 2 SUBUNIT
BETA-GALACTOSIDASE
BETA-GLUCOSIDASE
CXE CARBOXYLESTERASE
CYCLO-DOPA 5-O-GLUCOSYLTRANSFERASE
CYCLOPHILIN-LIKE PEPTIDYL-PROLYL CIS-TRANS ISOMERASE
CYTIDINE/DEOXYCYTIDYLATE DEAMINASE
CYTOCHROME C OXIDASE SUBUNIT VIB
CYTOCHROME P450
CYTOCHROME P450
CYTOCHROME P450
DIENELACTONE HYDROLASE
DIHYDROLIPOYL DEHYDROGENASE
DISTACHYON 3-HYDROXYBENZOATE 6-HYDROXYLASE
FAD/NAD(P)-BINDING OXIDOREDUCTASE
FERRIC REDUCTION OXIDASE
GLUTATHIONE PEROXIDASE
GLYCOGENIN DOMAIN-CONTAINING PROTEIN
GLYCOGENIN-LIKE STARCH INITIATION PROTEIN
HISTIDINOL PHOSPHATE PHOSPHATASE
HISTIDYL-TRNA SYNTHETASE
INORGANIC PYROPHOSPHATASE
ISOAMYLASE
ISOMERASE
L-ALLO-THREONINE ALDOLASE
L-ASPARTATE OXIDASE
LYSINE-KETOGLUTARATE REDUCTASE
METHIONINE SULFOXIDE REDUCTASE
MONOOXYGENASE
MULTIPLE INOSITOL POLYPHOSPHATE PHOSPHATASE
NAD(P)H DEHYDROGENASE B2
NAD(P)H:QUINONE OXIDOREDUCTASE
NADP-DEPENDENT MALIC ENZYME
OXYSTEROL-BINDING FAMILY PROTEIN
OXYSTEROL-BINDING FAMILY PROTEIN
PLASMA MEMBRANE H+ ATPASE
PYRIDOXINE/PYRIDOXAMINE 5'-PHOSPHATE OXIDASE
QUINONE OXIDOREDUCTASE
16.628
7.443
2.865
3.159
4.017
2.259
5.05E-04
4.75E-04
1.16E-03
1.12E-03
5.89E-04
4.20E-03
2574.234
12504.224
772.089
1131.712
8536.978
6096.448
Glycine max
Arabidopsis thaliana
Vis vinifera
Eriobotrya japonica
Glycine max
Arabidopsis thaliana
3E-138
4E-175
0.0
0.0
6E-175
0.0
XM_003516359
NM_179581
XM_002274298
JF414121
XM_003533767
NM_124670
13.142
12.848
6.495
5.862
7.136
61.726
5.751
4.742
17.182
125.628
4.588
4.555
34.36
8.169
88.176
14.878
4.583
48.071
2.792
3.713
3.793
49.103
77.276
47.098
6.68
3.266
4.703
2.863
64.066
8.67
15.193
7.079
2.233
7.659
6.921
8.354
5.496
207.743
2.206
2.728
6.326
3.98
6.333
5.105
10.403
66.513
6.519
7.247
191.25
3.135
17.292
3.061
11.371
4
2.462
4.323
7.624
4.465
3.79E-04
4.74E-04
6.96E-04
1.49E-03
4.41E-04
4.41E-04
4.69E-04
5.72E-04
3.78E-04
1.03E-03
1.18E-03
2.04E-03
4.11E-04
5.45E-04
3.66E-04
3.91E-04
2.08E-03
4.03E-04
1.59E-03
3.42E-03
8.02E-04
5.32E-04
4.64E-04
4.65E-04
8.23E-04
1.41E-03
2.65E-03
1.95E-03
5.49E-04
1.04E-03
3.78E-04
6.48E-04
2.31E-03
1.70E-03
1.69E-03
4.73E-04
5.26E-04
8.21E-04
1.34E-03
1.49E-03
7.86E-04
1.87E-03
1.11E-03
5.29E-04
4.94E-04
4.33E-04
4.33E-04
6.20E-04
6.55E-04
7.64E-04
3.83E-04
1.57E-03
6.84E-04
1.37E-03
9.77E-04
7.65E-04
1.63E-03
9.97E-04
8335.241
9265.162
801.75
1233.291
66835.624
4279.458
15418.07
4718.315
54892.377
14135.73
5118.796
2645.553
2911.479
63827.81
27282.14
200929.78
2842.268
6923.693
2574.489
1102.949
780.564
9441.474
4636.072
13047.412
1799.053
3816.298
3792.767
4691.212
2846.156
4727.742
2049.247
1722.855
1849.618
1036.006
1110.972
1293.24
13073.956
1047.09
3517.21
1421.08
8138.59
4898.77
10679.243
1430.92
24302.978
1810.436
16450.421
51846.022
2535.825
4347.381
16333.61
1552.909
5967.093
961.383
1206.215
27517.153
2502.027
1945.12
Solanum lycopersicum
Arabidopsis lyrata
Populus trichocarpa
Populus trichocarpa
Populus trichocarpa
Populus trichocarpa
Medicago truncatula
Vis vinifera
Arabidopsis thaliana
Arabidopsis lyrata
Medicago truncatula
Nicoana plumbaginifolia
Arabidopsis thaliana
Fragaria x ananassa
Cicer arienum
Fragaria x ananassa
Arabidopsis thaliana
Vis vinifera
Medicago truncatula
Vis vinifera
Glycine max
Medicago truncatula
Lotus japonicus
Malus pumila
Mirabilis jalapa
Arabidopsis thaliana
Zea mays
Arabidopsis thaliana
Populus trichocarpa
Citrus sinensis
Arabidopsis thaliana
Arabidopsis thaliana
Vis vinifera
Brachypodium distachyon
Arabidopsis thaliana
Malus domesca
Pisa straotes
Medicago truncatula
Arabidopsis thaliana
Prunus mume
Arabidopsis thaliana
Glycine max
Solanum tuberosum
Medicago truncatula
Glycine max
Arabidopsis thaliana
Gossypium hirsutum
Fragaria x ananassa
Arabidopsis lyrata
Medicago truncatula
Arabidopsis thaliana
Solanum tuberosum
Bean (P.vulgaris)
Vis vinifera
Arabidopsis lyrata
Prunus persica
Solanum lycopersicum
Glycine max
5E-113
2E-156
2E-34
6E-105
1E-98
0.0
1E-128
1E-144
8E-127
5E-111
0.0
2E-42
1E-39
0.0
8E-154
0.0
7E-139
0.0
0.0
0.0
0.0
0.0
1E-143
3E-141
2E-148
1E-57
2E-92
2E-41
1E-59
2E-78
8E-45
5E-42
0.0
6E-82
5E-72
0.0
8E-13
0.0
0.0
0.0
0.0
4E-86
0.0
9E-117
0.0
0.0
0.0
2E-116
4E-90
0.0
0.0
7E-78
0.0
0.0
0.0
0.0
0.0
3E-29
XM_004230521
XM_002866557
XM_002309556
XM_002324800
XM_002298091
XM_002330233
XM_003620308
XM_002264706
NM_128618
XM_002865047
XM_003629897
AJ234901
NM_111199
AF039182
XM_004494635
AY703448
NM_118352
XM_002279862
XM_003624606
XM_002274041
XM_003556532
XM_003630403
EU710846
DQ279907
AB182643
NM_102458
EU974505
NM_125166
XM_002299543
AF426451
NM_148854
NM_113263
XM_002276817
XM_003581183
NM_120614
XP_008373357
0.0
XM_003526736
SECONDARY METABOLISM
gene27475
QUINONE OXIDOREDUCTASE
gene21391
QUINONE OXIDOREDUCTASE
gene18229
gene06906
gene19545
13.233
EF620783
XM_003608665
NM_106363
XP_008237177
NM_111144.5
XM_003531579
AY132998
XM_003590624
XM_003521724
NM_121480
AF264147
Z69596
XM_002868137
XM_003600923
NM_116741
AB061251
J03825
XM_002283398
XM_002872324
AJ271438
XM_004236102
XM_003531961
5.39E-04
5.816
4.69E-04
3E-151
22.715
3.80E-04
9E-146
AK221446
NM_120332
137.527
1.97E-03
1E-69
XM_003589612
3E-105
XM_003594254
2.11E-03
gene09668
S-ADENOSYLMETHIONINE SYNTHETASE
5.368
7.16E-04
0.0
gene19647
S-ADENOSYLMETHIONINE-DEPENDENT METHYLTRANSFERASE
35.764
3.98E-04
1.00E-91
gene19469
S-ADENOSYLMETHIONINE-DEPENDENT METHYLTRANSFERASE
36.527
6.24E-04
3E-107
XM_003624980
gene12180
S-ADENOSYLMETHIONINE-DEPENDENT METHYLTRANSFERASE
11.05
4.00E-04
7E-105
NM_ 121121
gene30813
S-ADENOSYLMETHIONINE-DEPENDENT METHYLTRANSFERASE
6.439
6.13E-04
gene12002
9.123
1.05E-03
0.0
AJ251970
gene26251
S-METHYL-5-THIORIBOSE KINASE
2.287
5.15E-03
0.0
NM_103869
gene22780
3.963
5.73E-04
7E-115
HM068618
gene24860
TREHALOSE-PHOSPHATE SYNTHASE
gene09373
gene20126
UDP-ARABINOSE 4-EPIMERASE
gene32119
UDP-GLUCOSE 4-EPIMERASE
7.433
3E-136
XM_003625634
NM_129701
EU955451
26.578
7.73E-04
0.0
2.154
2.105
3.82E-03
3.20E-03
0.0
0.0
XM_003524972
0.0
XM_003610933
2.771
2.83E-03
gene16762
UDP-GLUCOSE:STEROL 3-O-GLUCOSYLTRANSFERASE
12.073
4.83E-04
gene07097
10.098
3.90E-04
gene21168
gene04078
WD-REPEAT PROTEIN
XYLOSE ISOMERASE
12.423
4.999
1.98E-03
7.00E-04
gene21964
gene17534
gene06716
gene24970
gene03258
0.0
NM_106505
XM_002272055
EU342378
XP_010100274
4E-44
0.0
0.0
XM_002510961
XM_003610131
3E-144
1E-112
0.0
1E-174
2E-119
XP_008351630
DQ279909
XM_002319738
XM_003612930
XM_002867470
CLUSTER UP(ABA+AUX0)
SECONDARY METABOLISM
2.913
15.428
45.817
2.525
2.26
1.68E-03
3.80E-04
7.31E-05
1.86E-03
1.28E-03
4567.83
4299.122
3399.351
4289.28
9598.769
Malus domesca
Malus pumila
Populus trichocarpa
Medicago truncatula
Arabidopsis lyrata subsp. lyrata
Agius, F. 2003
Almeida, JR. 2007
(continued)
Primary and Secondary Metabolism
GENES
Putave funcon
p-value
Up regulated
a.u.i.
e-value
2E-69
7E-168
1E-61
4E-169
2E-124
0.0
2E-149
0.0
0.0
2E-84
6E-156
0.0
3E-44
0.0
9E-45
1E-125
0.0
1E-171
0.0
0.0
0.0
5.00E-95
NM_106063
XP_002330269
XM_002298093
XM_002330233
XM_003619657
AF452450
DQ279906
EOY28772
XM_002307093
XM_002303510
GU590869
XM_002315974
NM_103710
XP_008241785
XP_003591094
NM_001202723
XP_009358973
XP_009351796
XM_003621562
FJ415190
NM_124400
NM_121121
0.0
XP_008227530
0.0
4E-138
0.0
0.0
4E-142
0.0
0.0
0
0.0
0.0
0.0
2E-115
0.0
1E-114
6E-123
0
0.0
0.0
1E-159
0.0
2E-101
1E-156
2E-111
3E-92
XP_008383990
NM_101878
XP_009352311
AHD24944
XM_004140350
XP_008218253
XP_009368303
XM_002268277
XP_008237950
XP_009366842
ABW38332
XM_003554028
XP_008350011
JN573600
XP_009365718
XM_003618131
FJ752239
NM_113698
AB426519
XM_002530324
NM_102067
XP_009345225
XP_008445030
XM_002271457
XM_002533353
NM_124635
Reference
CLUSTER UP(ABA0AUX-)
SECONDARY METABOLISM
gene20258
gene31922
gene11730
gene31923
gene17851
gene19636
gene28530
gene19490
gene06729
gene07140
gene09988
gene29956
gene17572
gene14886
gene28497
gene02043
gene17390
gene00617
gene14916
gene26275
gene09966
gene32447
2-ISOPROPYLMALATE SYNTHASE
2-OXOGLUTARATE (2OG) AND FE(II)-DEPENDENT OXYGENASE
2-OXOGLUTARATE (2OG) AND FE(II)-DEPENDENT OXYGENASE
2-OXOGLUTARATE (2OG) AND FE(II)-DEPENDENT OXYGENASE
4,5-DOPA DIOXYGENASE EXTRADIOL PROTEIN
ADENOSINE 5'-PHOSPHOSULFATE REDUCTASE
CARBOXYLESTERASE
CORE-2/I-BRANCHING BETA-1,6-N-ACETYLGLUCOSAMINYLTRANSFERASE FAMILY PROTEIN
CYTOCHROME P450
CYTOCHROME P450
CYTOCHROME P450
CYTOCHROME P450
DOLICHYL-PHOSPHATE MANNOSYLTRANSFERASE POLYPEPTIDE
ESTERASE-LYPASE DOMAIN CONTAINING PROTEIN
GLUCOSE AND RIBITOL DEHYDROGENASE
MOLYBDOPTERIN BIOSYNTHESIS PROTEIN
MONOCOPPER OXIDASE
NON-FUNCTIONAL NADPH-DEPENDENT CODEINONE REDUCTASE 2-LIKE
OXIDOREDUCTASE N-TERMINAL DOMAIN CONTAINING PROTEIN
PHOSPHOGLYCERATE DEHYDROGENASE
QUINOLINATE SYNTHASE
gene16110
S-ADENOSYLMETHIONINE-DEPENDENT METHYLTRANSFERASE
SENESCENCE-ASSOCIATED CARBOXYLESTERASE 101 ISOFORM X2
gene10140
gene06823
gene07049
gene30068
gene13960
gene34982
gene27413
gene33290
gene12400
gene12401
gene08033
gene10225
gene27225
gene31672
gene22014
gene25602
gene13709
gene11100
gene01456
gene14712
gene22089
gene17051
gene08799
gene34103
gene17266
gene08633
2.449
18.23
14.39
32.47
2.848
7.41
3.559
4.70
355.48
57.82
35.50
8.78
3.078
2.386
12.71
6.17
2.783
41.70
3.419
4.72
17.57
22.70
4.00
3.45E-03
1.63E-03
7.39E-04
3.83E-04
2.59E-03
4.20E-04
9.22E-04
1.31E-03
1.90E-03
3.83E-04
7.16E-04
1.10E-03
1.13E-03
1.47E-03
5.16E-04
2.44E-04
1.37E-03
4.22E-04
1.17E-03
7.52E-03
8.35E-04
5.81E-04
1.10E-03
937.24
2129.666
1624.766
12119.73
17161.69
7605.394
1161.15
733.325
2966.733
3211.294
726.525
1495.191
1931.15
2904.33
772.58
2398.752
2557.98
5519.18
5612.41
4746.82
2923.164
1286.25
Arabidopsis thaliana
Populus trichocarpa
Populus trichocarpa
Populus trichocarpa
Medicago truncatula
Glycine max
Malus pumila
Theobroma cacao
Populus trichocarpa
Populus trichocarpa
Nicoana tabacum
Populus trichocarpa
Arabidopsis thalian
Prunus mume
Medicago truncatula
Arabidopsis thaliana
Pyrus x bretschneideri
Pyrus x bretschneideri
Medicago truncatula
Gossypium hirsutum
Arabidopsis thaliana
Arabidopsis thaliana
CLUSTER UP(ABA0AUX0)
3.169
8.17
2.551
2.64
4.43
4.689
3.218
3.499
2.353
2.316
3.567
3.416
2.578
1226.608
3
2.573
2.492
2.487
2.347
2.564
4.009
2.33
2.219
2.284
3.83E-03
1.52E-03
1.22E-03
2.24E-03
6.04E-04
3.39E-03
1.17E-03
1.14E-03
1.32E-03
5.69E-04
3.46E-03
7.60E-04
1.25E-03
5.20E-05
3.42E-02
1.57E-03
2.41E-03
1.90E-03
3.57E-03
2.16E-03
7.99E-03
4.52E-03
1.48E-03
1.66E-03
2.246
2.151
1.23E-03
7.79E-03
polysaccharides, polynucleotides, etc. This methylation is fundamental for a large number of important biological functions
(Mata 2007; Hugueney et al. 2009). In our transcriptomic study,
we have detected several genes encoding both types of enzymes
(Table 10; Table S24), indicating that O-methylation process of
many metabolites, as flavonoids and phenylpropanoids, is important in ripe fruits.
Conclusion
Our data show that auxin is the main hormone regulating
the expression of genes implied in the initial development
and growth of the strawberry fruit, and that ABA is regulating the expression of genes implied in the final maturation and ripening. These data also strongly support the
proposal of (Perkins-Veazie 1995) which suggested that a
determined ratio of auxins/ABA is the main regulatory signal that triggers the events required to promote the maturation and ripening stages once the strawberry fruit is already developed. However, it cannot be ruled out that other
hormonal or physiological signals, not yet elucidated, can
influence some aspects of the strawberry fruit growth and
ripening process.
760.79
990.485
909.16
10890.92
819.10
3963.77
23434.35
16455.963
6762.14
7301.02
3544.80
18652.533
1143.48
27385.95
1377.74
7956.769
23782.809
1116.262
5706.181
714.13
1573.448
777.38
23217.95
3636.73
Malus domesca
Arabidopsis thaliana
Pyrus x bretschneideri
Rosa rugosa
Cucumis savus
Prunus mume
Pyrus x bretschneideri
Vis vinifera
Prunus mume
Pyrus x bretschneideri
Fragaria x ananassa
Glycine max
Malus domesca
Malus x domesca
Pyrus x bretschneider
Medicago truncatula
Malus x domesca
Arabidopsis thaliana
Rosa x damascena
Rosa x damascena
Arabidopsis thaliana
Pyrus x bretschneideri
Cucumis melo
Vis vinifera
4E-112
0.0
non-uniformities in a scanned image were determined as outliers and thus excluded from downstream analyses.
The microarray data were analysed with the software for
gene expression analysis ArrayStar 5 (DNASTAR). Raw expression intensities obtained from each one biological replica
were normalized through the Robust Multichip Average
(RMA) method. Moderated t test and false discovery rate
(FDR) (Benjamini and Hochberg 1995), for multiple testing
corrections, were used with an adjusted p < 0.01 to statistically
identify significant differences. The correlation coefficients (r value) and coefficients of determination (r2) for
the signals obtained in each of the biological replicates and
conditions were calculated by fitting the normalized data to
a linear mode with the lm() function implemented under
the R language.
Treemaps were performed by the Macrofocus TreeMap program, grouping genes by general functions, and representing
the fold change values by a scale of colour taking into account
that any level higher than 30-fold changes is considered saturated and therefore is drawn in the treemap with the same dark
colour. Actual fold change values shown are detailed in the
corresponding tables. There is an interactive version of the
treemap available under request that will allow the examination of the actual genes names and fold change values.
Annotation of sequences from the EST library
Blast2GO v 2.7.2 suite was used for functional annotation of
the EST sequences using BLASTX with an expected value
cutoff of 1.0E-10 (Conesa et al. 2005). Only genes that were
over- and under-expressed more than 2-fold in the microarray
analysis were used. GO data for each sequence was enriched
used ANNEX (Annotation Augmentation) and with information of the InterPro database. Graphics from GO data were
also obtained with this suite.
Gene ID shown in all of the tables and figures are those
reported in the F. vesca Genome Database (http://www.
strawberrygenome.org/).
Validation of microarray data and expression analysis
by quantitative real-time PCR
Expression analyses of genes herein analyzed and studied in all
physiological conditions were performed by quantitative realtime PCR (qRT-PCR) using an iCycler device (BioRad) as
previously described (Bentez-Burraco et al. 2003). Firststrand cDNA was obtained from 2 g total RNA using the
iScript kit (BioRad), following manufacturer instructions. An
additional table depicts the primer sequences used for quantitative amplification (Table S1). Each reaction was performed by
triplicate, and the corresponding Ct values were normalized
using the Ct value corresponding to an interspacer 26S18S
strawberry RNA gene (Bentez-Burraco et al. 2003; Raab
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