Table 2.
Summary of the most significant candidate genes for monoterpene biosynthesis.
| Non-redundant V1 gene prediction ID | Functional annotation | Evidences from the present work | Evidences from the literature |
|---|---|---|---|
| Cluster 4 (free HO-diendiol II, bound linalool, geraniol, nerol, trans/cis-8-HO-linalool, OxA, OxC, OxD, HO-diendiol I + HO-trienol, HO-diendiol II, rose oxide I and II) | |||
| VIT_01s0026g01970 | RNA-binding region RNP-1 (RNA recognition motif) | Correlated with VIT_02s0012g01630, VIT_05s0062g00430, VIT_05s0062g00520 and additional candidate genes in Supplementary Table S9 Down-regulated at stages 2–5 with respect to stage 1 |
§ Ruwe et al., 2011 # Battilana et al., 2009 |
| VIT_02s0012g01040* | NAC domain-containing protein 71 | Correlated with VIT_06s0009g01140 and an additional candidate gene in Supplementary Table S9 Correlated with free OxC, bound linalool, trans-8-HO linalool, OxA, HO-diendiol I and II, rose oxide I and II Up-regulated at stages 2-5 with respect to stage 1 (array and qRT-PCR) |
# Doligez et al., 2006; Battilana et al., 2009; Lijavetzky et al., 2012; Palumbo et al., 2014 |
| VIT_02s0234g00100 | Ubiquitinyl hydrolase 1 | Correlated with VIT_08s0007g05210, VIT_10s0003g00880 and additional candidate genes in Supplementary Table S9 Correlated with several bound monoterpenes Up-regulated at stage 5 with respect to stage 1 |
- |
| VIT_04s0023g00130* | Unknown protein | Positive correlation with free OxC, bound OxA, HO-diendiol I, rose oxide I and II Up-regulated at stages 4 and 5 with respect to stage 1 (array), at stage 5 with respect to stage 1 (qRT-PCR) |
# Battilana et al., 2009; Lijavetzky et al., 2012; Palumbo et al., 2014 |
| VIT_04s0023g02950 | Zinc finger (CCCH-type) family protein | Correlated with VIT_02s0012g01630, VIT_05s0062g00430, VIT_05s0062g00520 and additional candidate genes in Supplementary Table S9 Correlated with bound OxC Down-regulated at stages 2–4 with respect to stage 1 |
# Battilana et al., 2009; Lijavetzky et al., 2012 |
| VIT_06s0009g01140* | Amino acid permease | Correlated with free linalool, trans-8-HO-linalool, α-terpineol, HO-diendiol II, rose oxide I, bound linalool, geraniol, nerol, cis-8-HO-linalool, citronellol Up-regulated at stages 2-5 with respect to stage 1 (array and qRT-PCR) |
# Battilana et al., 2009; Palumbo et al., 2014; VTCdb |
| VIT_07s0031g01320 | TGA-type basic leucine zipper protein TGA1.1 | Correlated with VIT_02s0012g01630, VIT_05s0062g00430, VIT_05s0062g00520, VIT_00s0389g00030, VIT_00s0389g00040 and additional candidate genes in Supplementary Table S9 Correlated with bound trans-8-HO-linalool, OxD, HO-diendiol II Down-regulated at stages 2-5 with respect to stage 1 |
# Cramer et al., 2014; Wen et al., 2015 |
| VIT_07s0031g01930* | Myb TKI1 (TSL-kinase interacting protein 1) | Correlated with VIT_06s0009g01140 and additional candidate genes in Supplementary Table S9 Correlated with several monoterpenes (free linalool with high significance) Up-regulated at stages 2-5 with respect to stage 1 (array), at stages 4 and 5 with respect to stage 1 (qRT-PCR) |
# Lijavetzky et al., 2012; Palumbo et al., 2014 |
| VIT_08s0040g03040 | Glutathione S-transferase GSTO1 | Correlated with bound trans-8-HO-linalool, OxD, trans-geranic acid, α-terpineol, HO-diendiol II Up-regulated at stage 5 with respect to stage 1 |
# VTCdb |
| VIT_09s0054g01780 | HAC1 (P300/CBP acetyltransferase-related protein 2 gene) | Correlated with VIT_04s0023g02610 Correlated with bound trans-8-HO-linalool, rose oxide II Up-regulated at stages 3-5 with respect to stage 1 |
§ (Shen et al., 2015) |
| VIT_10s0003g00880* | Nudix hydrolase 15 | Correlated with bound trans-8-HO-linalool and OxC Up-regulated at stage 4 with respect to stage 1 (qRT-PCR) |
§ Magnard et al., 2015 |
| VIT_12s0028g03860* | Zinc finger (C3HC4-type ring finger) protein (RMA1) | Correlated with VIT_10s0003g00880 Correlated with bound OxC Up-regulated at stages 4 and 5 with respect to stage 1 (array), at stage 2 with respect to stage 1 (qRT-PCR) |
# Battilana et al., 2009; Lijavetzky et al., 2012; Palumbo et al., 2014; VTCdb |
| VIT_14s0066g01090* | Myb domain protein 24 | Correlated with VIT_18s0001g04280 and VIT_18s0001g04530 Correlated with bound OxC Up-regulated at stage 5 with respect to stage 1 (array) |
# Battilana et al., 2009; Carbonell-Bejerano et al., 2014b; Savoi et al., 2016; Wong et al., 2016 |
| VIT_18s0001g13790 | Cytochrome P450, family 83, subfamily B, polypeptide 1 (CYP71) | Correlated with several oxidized monoterpenes (bound cis/trans 8-HO-linalool, OxA, OxD, trans-geranic acid, HO-diendiol I and II) In the same biclusters as free cis-8-HO-linalool, OxB, trans-geranic acid, HO-diendiol I + HO-trienol Up-regulated at stages 3-5 with respect to stage 1 |
§ Ginglinger et al., 2013 # Ilc et al., 2017 |
| VIT_19s0014g03300* | NAC domain containing protein 2 | Correlated with VIT_04s0023g02610 and VIT_10s0003g00880 Correlated with bound trans-8-HO-linalool, OxC, rose oxide II Up-regulated at stage 5 with respect to stage 1 (array) |
§ Giovannoni, 2004; Nieuwenhuizen et al., 2015 # Lijavetzky et al., 2012; Blanco-Ulate et al., 2015 |
| VIT_00s0214g00090* | F-box protein PP2-B10 (Protein phloem protein 2-like B10) | Correlated with VIT_06s0009g01140, VIT_15s0048g01490 and additional candidate genes in Supplementary Table S9 Correlated with several monoterpenes Up-regulated at stages 3–5 with respect to stage 1 (array), at stage 4 with respect to stage 1 (qRT-PCR) |
# Battilana et al., 2009; Palumbo et al., 2014 |
| Cluster 6 (free geraniol, nerol, bound trans-geranic acid, α-terpineol, 4-terpineol) | |||
| VIT_02s0012g01240 | PHD finger transcription factor | Correlated with VIT_06s0009g01140 and VIT_08s0007g05210 Correlated with free geraniol, bound α-terpineol Up-regulated at stage 5 with respect to stage 1 |
# Doligez et al., 2006; Battilana et al., 2009 |
| VIT_08s0007g05210 | Amino acid permease | Correlated with free geraniol and bound α-terpineol Up-regulated at stage 5 with respect to stage 1 |
# Battilana et al., 2009; VTCdb |
| VIT_15s0048g02410 | Myb CCA1 (circadian clock associated 1) | Down-regulated at stage 4 with respect to stage 1 | § Vranová et al., 2012 # VTCdb |
| Cluster 9 (free linalool, OxB, OxC) | |||
| VIT_02s0012g01630 | Transmembrane protein 41B (SNARE associated Golgi protein) | Down-regulated at stages 2-5 with respect to stage 1 | § Ting et al., 2015 # Doligez et al., 2006; Battilana et al., 2009 |
| VIT_04s0008g05210* | BZIP protein HY5 (HY5) | Correlated with VIT_06s0009g01140 Up-regulated at stages 4 and 5 with respect to stage 1 (array) |
§ Liu et al., 2004; Toledo-Ortiz et al., 2014; Zhou et al., 2015 # Carbonell-Bejerano et al., 2014a,b; Cramer et al., 2014; Liu et al., 2015; Loyola et al., 2016 |
| VIT_04s0023g01250 | Brassinosteroid signaling positive regulator (BZR1) | Correlated with VIT_02s0012g01630, VIT_00s0389g00030, VIT_00s0389g00040 and additional candidate genes in Supplementary Table S9 Correlated with free OxB Down-regulated at stage 2, 3 and 5 with respect to stage 1 |
§ Liu et al., 2014 # Battilana et al., 2009; Fortes et al., 2015 |
| VIT_06s0004g07550* | Wound-induced protein WI12 | Correlated with VIT_06s0009g01140 and an additional candidate gene in Supplementary Table S9 Correlated with free OxC, HO-diendiol II, bound linalool, geraniol, nerol, OxA, citronellol, HO-diendiol I, rose oxide I Up-regulated at stages 2-5 with respect to stage 1 (array), at stages 2, 4 and 5 with respect to stage 1 (qRT-PCR) |
# Battilana et al., 2009; Lijavetzky et al., 2012; Palumbo et al., 2014; VTCdb |
| VIT_07s0104g01050 | Homeobox protein | Correlated with VIT_06s0009g01140 and an additional candidate gene in Supplementary Table S9 Correlated with several monoterpenes Up-regulated at stages 4 and 5 with respect to stage 1 |
- |
| VIT_08s0007g05880 | Dehydration-induced protein (ERD15) | Correlated with VIT_02s0012g01630, VIT_05s0062g00430, VIT_05s0062g00520, VIT_15s0048g01590, VIT_00s0389g00030, VIT_00s0389g00040 and additional candidate genes in Supplementary Table S9 Down-regulated at stages 2-5 with respect to stage 1 |
# Koundouras et al., 2006; Battilana et al., 2009; Savoi et al., 2016 |
| Other clusters | |||
| VIT_10s0003g03190* | RNA recognition motif (RRM)-containing | Correlated with VIT_06s0009g01140 and an additional candidate gene in Supplementary Table S9 Up-regulated at stages 2–5 with respect to stage 1 (array) |
# Battilana et al., 2009; Lijavetzky et al., 2012; VTCdb |
| VIT_16s0100g00400 | Ethylene-responsive transcription factor ERF025 | Correlated with VIT_02s0012g01630, VIT_05s0062g00430, VIT_05s0062g00520, VIT_00s0389g00030, VIT_00s0389g00040 and additional candidate genes in Supplementary Table S9 Down-regulated at stages 3-5 with respect to stage 1 |
# Palumbo et al., 2014; VTCdb |
| VIT_18s0001g05250 | DREB sub A-6 of ERF/AP2 transcription factor (RAP2.4) | Correlated with VIT_02s0012g01630, VIT_05s0062g00430, VIT_05s0062g00520, VIT_15s0048g01590, VIT_00s0389g00030, VIT_00s0389g00040 and additional candidate genes in Supplementary Table S9 Down-regulated at stages 2-5 with respect to stage 1 |
# Wen et al., 2015 |
| VIT_03s0038g02500 | SKP1 | Correlated with VIT_04s0023g02610 and VIT_10s0003g00880 Up-regulated at stage 5 with respect to stage 1 |
§ Devoto et al., 2002 # D'Onofrio et al., 2009; Gómez-Plaza et al., 2012; May and Wüst, 2015 |
| VIT_03s0063g02030* | 4-hydroxy-3-methylbut-2-enyl diphosphate reductase | In the same cluster as free OxA Up-regulated at stages 2, 4 and 5 with respect to stage 1 (qRT-PCR) |
§ Botella-Pavía et al., 2004 # Martin et al., 2012; Wen et al., 2015 |
| VIT_03s0180g00200 VIT_03s0180g00320 | Limonoid UDP-glucosyltransferase Indole-3-acetate beta-glucosyltransferase | In the same biclusters as bound OxC, 4-terpineol, HO-diendiol I + HO-trienol Down-regulated at stage 3 with respect to stage 1 |
§ Kita et al., 2000 # Bönisch et al., 2014a; Blanco-Ulate et al., 2015 |
| VIT_04s0023g02610* | Epoxide hydrolase 2 | Up-regulated at stage 5 with respect to stage 1 (array) | # Battilana et al., 2009; Savoi et al., 2016 |
| VIT_15s0046g01440 | BZip transcription factor G- box binding factor 3 | Negatively correlated with several monoterpenes Down-regulated at stages 3–5 with respect to stage 1 |
§ Sibéril et al., 2001 # Cramer et al., 2014 |
| VIT_15s0048g01490 | Geraniol 10-hydroxylase (CYP76) | In the same cluster as free OxD and rose oxide II In the same biclusters as free HO-diendiol I+ HO-trienol, bound OxC, HO-diendiol I + HO-trienol Up-regulated at stages 3 and 4 with respect to stage 1 |
§ Ginglinger et al., 2013; Höfer et al., 2014; Boachon et al., 2015 # Cramer et al., 2014; Ilc et al., 2017 |
| VIT_15s0048g01590 | CYP76B1 | In the same biclusters as free OxA Down-regulated at stage 3 with respect to stage 1 |
§ Ginglinger et al., 2013; Höfer et al., 2014; Boachon et al., 2015 # Ilc et al., 2017; VTCdb |
| VIT_16s0039g00010 | ABC transporter G member 7 | Up-regulated at stage 5 with respect to stage 1 | § Kang et al., 2011 # Cramer et al., 2014; VTCdb |
| VIT_16s0050g01580 | UDP-glucose: anthocyanidin 5,3-O-glucosyltransferase (VvGT7) | In the same biclusters as bound HO-diendiol I + HO-trienol Down-regulated at stages 3–5 with respect to stage 1 |
§ Caputi et al., 2008 # Doligez et al., 2006; Bönisch et al., 2014a; Friedel et al., 2016 |
| VIT_18s0001g04280 VIT_18s0001g04530 | (-)-germacrene D synthase | Up-regulated at stage 5 with respect to stage 1 | # Savoi et al., 2016 |
| VIT_18s0001g09230 | Salt tolerance zinc finger | Negatively correlated with bound 4-terpineol Down-regulated at stage 5 with respect to stage 1 |
§ Pauw et al., 2004 # Cramer et al., 2014 |
| VIT_00s0389g00030 VIT_00s0389g00040 | CYP72A1 | In the same clusters as free OxD, HO-diendiol I + HO-trienol, rose oxide II In the same biclusters as free HO-diendiol I + HO-trienol, bound OxC Down-regulated at stage 5 with respect to stage 1 |
# Doligez et al., 2006; Battilana et al., 2009; Cramer et al., 2014; VTCdb |
| VIT_00s0463g00020 | Scarecrow transcription factor 5 (SCL5) | Correlated with VIT_02s0012g01630, VIT_00s0389g00030, VIT_00s0389g00040 and additional candidate genes in Supplementary Table S9 Down-regulated at stages 2–5 with respect to stage 1 |
# Battilana et al., 2009; Wen et al., 2015 |
They were selected from the whole list of genes with a potential association to monoterpenes (based on their correlation with metabolites and/or membership to soft clusters/biclusters harboring metabolites) reported in Supplementary Table S9, giving priority to the genes with the biggest expression changes, supporting evidence from the literature (relevant function in other plant species, co-localization with QTLs for monoterpene content, coexpression with genes involved in the terpene pahway), profile consistency between microarray and qRT-PCR analyses (the genes assayed by both techniques are marked with an asterisk). The symbols # and § indicate references for grapevine and other plant species, respectively. For details, including the correspondence between microarray probes and V1 gene predictions, see Supplementary Table S9.