Positive Selection and Functional Divergence of R2R3-MYB Paralogous Genes Expressed in Inflorescence Buds of Scutellaria Species (Labiatae)
Abstract
:1. Introduction
Species | Pollen | Growth Form | |||
---|---|---|---|---|---|
Size (μm) | Exine | Stem | Inflorescence | Petal and Corolla | |
S. indica | (18–23) × (12–17) | Finely reticulate | Erect or procumbent at base | Terminal loose raceme | Geniculate at base, purple, pink or white |
S. tashiroi | (18–22) × (14–17) | Loose reticulate to rugulate | Slender, procumbent, tufted | Axillary, seldom terminal raceme | Curve at base, dark purple |
S. playfairii | (16–20) × (10–15) | Loose reticulate to rugulate | Erect, seldom tufted | Terminal loose raceme | Geniculate at base, whitish purple |
S. taiwanensis | (23–30) × (16–20) | Irregular rugulate | Erect, often tufted | Terminal loose raceme | Geniculate at base, white with purple spot |
Group | Function | Species | Reference |
---|---|---|---|
MYB2/7/11 | Shoot and axillary meristems formation | Arabidopsis thaliana (S14) a | [28] |
Flavonoid regulation through GA metabolism; regulate PAL, C4H, CHS, CHI and UFGT | Scutellaria baicalensis | [27] | |
MYB8 | Induction of anthocyanin accumulation | Arabidopsis thaliana (S6) a and Nicotiana tabacum | [29] |
Sharing similar expression pattern with C4H and CHS after GA treatment | Scutellaria baicalensis | [27] | |
MYB13/19 | Alternation of expression level of anthocyanin biosynthesis genes and pigment accumulation under cold stress | Arabidopsis thaliana (AtMYB3) | [12] |
Brassica oleracea | [30] | ||
Nicotiana tabacum | [31] | ||
MYB15 | Regulation of serine/threonine protein phosphatases to enhance salt or drought tolerance | Arabidopsis thaliana (AtMYB20) | [32,33] |
MYB16 | MicroRNA regulation and anther and pollen development | Arabidopsis thaliana (S18) a | [17] |
2. Results
2.1. Gene Annotation by Basic Local Alignment Search Tool (BLAST) Analyses
Group Name | Phylogenetic Grouping | tBLASTx to Arabidopsis | ||||||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|
Stas | Spla | Sind | Stai | Sbai | Smon | Amborella | Arabidopsis | Solanum | Oryza | Accession Number | E-Value | |
MYB16 | KP167623 | KP167610 | KP167603 | KP167617 | KF008651 | ATYL_2013395 | – | – | XM_004236340 | – | NM_111977 | 7 × 10−69 |
(Stas_9284) | (Spla_28842) | (Sind_28842) | (Stai_7654) | (SbMYB16) | (AtMYB65) | |||||||
MYB15 | KP167621 | KP167607 | KP167598 | – | KF008664 | ATYL_2028518 | XM_006837947 | NM_105294 | XM_004236642 | NM_001070300 | NM_105294 | 1 × 10−85 |
(Stas_14132) | (Spla_13224) | (Sind_16195) | (AtMYB20) | NM_001054563 | (AtMYB20) | |||||||
NM_121666 | NM_001063857 | |||||||||||
(AtMYB43) | NM_001068382 | |||||||||||
NM_001069653 | ||||||||||||
MYB8 | KP167618 | KP167606 | KP167604 | KP167613 | KF008657 | ATYL_2121808 | XM_006849579 | AF048841 | XM_004252468 | AF062915 | 3 × 10−57 | |
(AtMYB82) | (AtMYB90) | |||||||||||
NM_123397 | ||||||||||||
(AtMYB23) | – | |||||||||||
MYB2/7/11 | XM_006837947 | XM_004245674 | NM_001186451 | |||||||||
XM_004248305 | ||||||||||||
MYB11 | KP167619 | KP167609 | KP167600 | – | KF008660 | ATYL_2012934 | – | – | – | – | NM_125143 | 7 × 10−63 |
(SbMYB11) | (AtMYB36) | |||||||||||
MYB2/7 | – | KP167611 | KP167605 | KP167615 | KC990835 | ATYL_2108188/2121208 | – | – | – | – | AF062901 | 9 × 10−71 |
(SbMYB2) | (AtMYB68) | |||||||||||
KC990836 | ||||||||||||
(SbMYB7) | ||||||||||||
MYB13/19 | XM_006854550 | - | XM_004253144 | |||||||||
XM_004246040 | ||||||||||||
XM_004244680 | ||||||||||||
MYB13 | KP167622 | KP167608 | KP167601 | KP167616 | KF008662 | – | – | – | – | – | NM_112200 | 3 × 10−40 |
KP167599 | (SbMYB13) | (AtMYB5) | ||||||||||
MYB19 | KP167620 | KP167612 | KP167602 | KP167614 | KF008667 | ATYL_2029067 | – | – | – | – | NM_112200 | 1 × 10−61 |
(SbMYB19) | (AtMYB5) |
2.2. Phylogenetic Analyses
2.3. Codon-Specific Positive Selection
Model | AtMYB5-Like | S6 | S14 | AtMYB20 | S18 | |||
---|---|---|---|---|---|---|---|---|
MYB 19 | MYB 13 | MYB 8 | MYB 7 | MYB 11 | MYB 15 | MYB 16 | ||
M1a | lnL | −1869.28 | −1419.48 | −2050.95 | −1685.91 | −1763.79 | −1803.50 | −2587.30 |
M2a | lnL | −1869.28 | −1419.24 | −2050.84 | −1685.59 | −1761.03 | −1802.53 | −2584.73 |
2ΔL | 0 | 0.49 | 0.22 | 0.63 | 5.52 | 1.94 | 5.13 | |
p | 1 | 0.391 | 0.449 | 0.364 | 0.032 | 0.19 | 0.038 | |
M7 | lnL | −1869.74 | −1419.61 | −2051.38 | −1686.13 | −1764.06 | −1804.13 | −2587.32 |
M8 | lnL | −1869.28 | −1419.24 | −2050.84 | −1685.59 | −1762.24 | −1802.53 | −2584.74 |
2ΔL | 0.92 | 0.74 | 1.07 | 1.07 | 3.63 | 3.2 | 5.17 | |
p | 0.491 | 0.345 | 0.293 | 0.293 | 0.082 | 0.101 | 0.038 | |
M8a | lnL | −1869.28 | −1419.48 | −2050.95 | −1685.91 | −1763.80 | −1803.51 | −2587.34 |
M8 | lnL | −1869.28 | −1419.24 | −2050.84 | −1685.59 | −1762.24 | −1802.53 | −2584.74 |
2ΔL | 0 | 0.49 | 0.22 | 0.63 | 3.11 | 1.96 | 5.19 | |
p | 0.5 | 0.447 | 0.755 | 0.365 | 0.048 | 0.107 | 0.013 |
2.4. Cluster-Specific Positive Selection and Functional Divergence
Background | Amborella | Arabidopsis | Oryza | Solanum | ||||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|
M1a (Null model) | ||||||||||||
np | 101 | 113 | 109 | 121 | ||||||||
lnL | −2402.594 | −2695.469 | −2735.734 | −3170.464 | ||||||||
Site class | Class 0 | Class 1 | Class 0 | Class 1 | Class 0 | Class 1 | Class 0 | Class 1 | ||||
Proportion | 0.938 | 0.062 | 0.869 | 0.131 | 0.824 | 0.176 | 0.99999 | 0.00001 | ||||
ω | 0.042 | 1 | 0.041 | 1 | 0.042 | 1 | 0.039 | 1 | ||||
Clade Model C | ||||||||||||
np | 110 | 122 | 118 | 130 | ||||||||
lnL | −2321.832 | −2606.658 | −2656.505 | −3059.730 | ||||||||
Site class | Class 0 | Class 1 | Class 2 | Class 0 | Class 1 | Class 2 | Class 0 | Class 1 | Class 2 | Class 0 | Class 1 | Class 2 |
Proportion | 0.698 | 0 | 0.302 | 0.710 | 0 | 0.290 | 0.676 | 0.034 | 0.290 | 0.687 | 0 | 0.313 |
ωBackground | 0.010 | 1 | 0.154 | 0.013 | 1 | 0.183 | 0.014 | 1 | 0.285 | 0.010 | 1 | 0.134 |
ωMYB2/7 | 0.010 | 1 | 0.062 | 0.013 | 1 | 0.101 | 0.014 | 1 | 0.040 | 0.010 | 1 | 0.045 |
ωMYB11 | 0.010 | 1 | 0.037 | 0.013 | 1 | 0.196 | 0.014 | 1 | 0.097 | 0.010 | 1 | 0.056 |
ωMYB15 | 0.010 | 1 | 0.028 | 0.013 | 1 | 0.000 | 0.014 | 1 | 0.017 | 0.010 | 1 | 0.000 |
ωMYB16 | 0.010 | 1 | 0.207 | 0.013 | 1 | 0.114 | 0.014 | 1 | 0.085 | 0.010 | 1 | 0.039 |
ωMYB8 | 0.010 | 1 | 0.054 | 0.013 | 1 | 0.058 | 0.014 | 1 | 0.029 | 0.010 | 1 | 0.160 |
ωMYB13 | 0.010 | 1 | 0.000 | 0.013 | 1 | 0.000 | 0.014 | 1 | 0.000 | 0.010 | 1 | 0.000 |
ωMYB19 | 0.010 | 1 | 999 | 0.013 | 1 | 999 | 0.014 | 1 | 999 | 0.010 | 1 | 999 |
LRT | ||||||||||||
2ΔL | 161.525 | 177.623 | 158.457 | 221.469 | ||||||||
df | 9 | 9 | 9 | 9 | ||||||||
p | 3.58 × 10−30 | 1.59 × 10−33 | 1.55 × 10−29 | 1.03 × 10−42 |
Model | np | lnL | Parameter | Class 0 | Class 1 | Class 2a | Class 2b |
---|---|---|---|---|---|---|---|
Model A ω = 1 fixed | 82 | −1486.769 | Proportion | 0.7630 | 0.1728 | 0.0523 | 0.0119 |
Background ω | 0.0285 | 1 | 0.0285 | 1 | |||
Foreground ω | 0.0285 | 1 | 1 | 1 | |||
Model A | 83 | −1484.552 | Proportion | 0.7930 | 0.1798 | 0.0222 | 0.0050 |
Background ω | 0.0292 | 1 | 0.0292 | 1 | |||
Foreground ω | 0.0292 | 1 | 11.1973 | 11.1973 | |||
LRT a | 2ΔL = 4.434, p = 0.0176 |
Type-I Functional Divergence | Type-II Functional Divergence | ||||
---|---|---|---|---|---|
Parameter | MYB19 vs. MYB13 | MYB7/11 vs. MYB2 | Parameter | MYB19 vs. MYB13 | MYB7/11 vs. MYB2 |
θI | 1.021 | −0.413 | θII | 0.052 | 0.125 |
SE θI | 0.161 | 0.293 | SE θII | 0.036 | 0.072 |
p of θI Z-score | <0.00001 | 0.099 | p of θII Z-score | 0.073 | 0.042 |
θIML | 0.999 | 0.006 | aR/πR | 1.405 | 1.869 |
AlphaML | 0.006 | 0.126 | GR/GC | 1 | 0.864 |
SE θI | 0.234 | 0.050 | F00,N | 0.927 | 0.727 |
LRT θI | 18.289 | 0.003 | F00,R | 0.018 | 0.036 |
p of LRT θI | 1.898 × 10−5 | 0.956 | F00,C | 0.018 | 0.091 |
3. Discussion
3.1. Diversification of R2R3-MYBs in Scutellaria Expressed in Inflorescence Buds
3.2. Phylogenetic Analyses and Functional Annotation
3.3. Positive Selection on Scutellaria MYB11 and MYB16
3.4. Different Types of Functional Divergence between Recent Duplicated Paralogs in Scutellaria R2R3-MYBs
4. Experimental Section
4.1. Data Collection, de Novo Transcriptome Assembly, and Annotation
4.2. Detecting Positive Selection
4.3. Functional Divergence Analyses
5. Conclusions
Supplementary Materials
Acknowledgments
Author Contributions
Conflicts of Interest
References
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Huang, B.-H.; Pang, E.; Chen, Y.-W.; Cao, H.; Ruan, Y.; Liao, P.-C. Positive Selection and Functional Divergence of R2R3-MYB Paralogous Genes Expressed in Inflorescence Buds of Scutellaria Species (Labiatae). Int. J. Mol. Sci. 2015, 16, 5900-5921. https://doi.org/10.3390/ijms16035900
Huang B-H, Pang E, Chen Y-W, Cao H, Ruan Y, Liao P-C. Positive Selection and Functional Divergence of R2R3-MYB Paralogous Genes Expressed in Inflorescence Buds of Scutellaria Species (Labiatae). International Journal of Molecular Sciences. 2015; 16(3):5900-5921. https://doi.org/10.3390/ijms16035900
Chicago/Turabian StyleHuang, Bing-Hong, Erli Pang, Yi-Wen Chen, Huifen Cao, Yu Ruan, and Pei-Chun Liao. 2015. "Positive Selection and Functional Divergence of R2R3-MYB Paralogous Genes Expressed in Inflorescence Buds of Scutellaria Species (Labiatae)" International Journal of Molecular Sciences 16, no. 3: 5900-5921. https://doi.org/10.3390/ijms16035900