# The paralogous R3 MYB proteins CAPRICE, TRIPTYCHON and ENHANCER OF TRY AND CPC1 play pleiotropic and partly non-redundant roles in the phosphate starvation response of Arabidopsis roots

**Authors:** Chun-Ying Chen, Wolfgang Schmidt

PMC · DOI: 10.1093/jxb/erv259 · Journal of Experimental Botany · 2015-05-28

## TL;DR

This study shows how three related R3 MYB proteins in Arabidopsis roots help plants respond to low phosphate levels by regulating various genes and processes.

## Contribution

The paper reveals new functions of R3 MYB proteins in phosphate starvation response and challenges the concept of genetic redundancy.

## Key findings

- Three R3 MYB proteins regulate root hair development and phosphate starvation response.
- Phosphate deficiency induces new roles in metal transport and membrane lipid remodelling.
- Environmental changes can assign unique functions to otherwise redundant proteins.

## Abstract

RNA sequencing of mutants defective in the expression of three paralogous MYB transcription factors revealed pleiotropic roles and dynamic shifts in the function of the proteins upon exposure to phosphate starvation.

Phosphate (Pi) deficiency alters root hair length and frequency as a means of increasing the absorptive surface area of roots. Three partly redundant single R3 MYB proteins, CAPRICE (CPC), ENHANCER OF TRY AND CPC1 (ETC1) and TRIPTYCHON (TRY), positively regulate the root hair cell fate by participating in a lateral inhibition mechanism. To identify putative targets and processes that are controlled by these three transcription factors (TFs), we conducted transcriptional profiling of roots from Arabidopsis thaliana wild-type plants, and cpc, etc1 and try mutants grown under Pi-replete and Pi-deficient conditions using RNA-seq. The data show that in an intricate interplay between the three MYBs regulate several developmental, physiological and metabolic processes that are putatively located in different tissues. When grown on media with a low Pi concentration, all three TFs acquire additional functions that are related to the Pi starvation response, including transition metal transport, membrane lipid remodelling, and the acquisition, uptake and storage of Pi. Control of gene activity is partly mediated through the regulation of potential antisense transcripts. The current dataset extends the known functions of R3 MYB proteins, provides a suite of novel candidates with critical function in root hair development under both control and Pi-deficient conditions, and challenges the definition of genetic redundancy by demonstrating that environmental perturbations may confer specific functions to orthologous proteins that could have similar roles under control conditions.

## Linked entities

- **Genes:** MISP (mitotic spindle positioning) [NCBI Gene 420097], ETC1 (Homeodomain-like superfamily protein) [NCBI Gene 838096], TRY (Homeodomain-like superfamily protein) [NCBI Gene 835401], CPC (Homeodomain-like superfamily protein) [NCBI Gene 819249], etc-1 (E3 ubiquitin-protein ligase etc-1) [NCBI Gene 174388], TRY (Homeodomain-like superfamily protein) [NCBI Gene 835401]
- **Proteins:** MISP (mitotic spindle positioning), ETC1 (Homeodomain-like superfamily protein), TRY (Homeodomain-like superfamily protein), CPC (Homeodomain-like superfamily protein), etc-1 (E3 ubiquitin-protein ligase etc-1), TRY (Homeodomain-like superfamily protein)
- **Chemicals:** phosphate (PubChem CID 1061)
- **Species:** Arabidopsis thaliana (taxon 3702)

## Full-text entities

- **Genes:** IRE (AGC (cAMP-dependent, cGMP-dependent and protein kinase C) kinase family protein) [NCBI Gene 836352] {aka INCOMPLETE ROOT HAIR ELONGATION, MMI9.15, MMI9_15}, GDPD2 (PLC-like phosphodiesterases superfamily protein) [NCBI Gene 834110] {aka AtGDPD2, MEE6.15, MEE6_15, glycerophosphodiester phosphodiesterase 2}, TCL2 (Homeodomain-like superfamily protein) [NCBI Gene 6240858] {aka TRICHOMELESS 2}, EXPA7 (expansin A7) [NCBI Gene 837813] {aka ATEXP7, ATEXPA7, ATHEXP ALPHA 1.26, EXP7, F5O11.30, F5O11_30}, AT4G26790 (GDSL-like Lipase/Acylhydrolase superfamily protein) [NCBI Gene 828786] {aka F10M23.130, F10M23_130}, RHS19 (root hair specific 19) [NCBI Gene 836876] {aka K8K14.13, K8K14_13, root hair specific 19}, ZIP4 (zinc transporter) [NCBI Gene 837640] {aka ATZIP4, T19D16.11, T19D16_11, zinc transporter 4 precursor}, IRT2 (iron regulated transporter 2) [NCBI Gene 827712] {aka ATIRT2, IRON REGULATED TRANSPORTER 2, T16H5.40, T16H5_40, iron regulated transporter 2}, PHT1;9 (phosphate transporter 1;9) [NCBI Gene 843976] {aka F15M4.7, phosphate transporter 1;9}, PAP25 (purple acid phosphatase 25) [NCBI Gene 829787] {aka ARABIDOPSIS THALIANA PURPLE ACID PHOSPHATASE 25, ATPAP25, F23E13.190, F23E13_190, purple acid phosphatase 25}, DRP4A (Dynamin related protein 4A) [NCBI Gene 842348] {aka Dynamin related protein 4A, F8A5.7, F8A5_7}, PLDALPHA1 (phospholipase D alpha 1) [NCBI Gene 820816] {aka PHOSPHOLIPASE D, PLD, phospholipase D alpha 1}, AT2G35640 (Homeodomain-like superfamily protein) [NCBI Gene 818133] {aka T20F21.22, T20F21_22}, PEPC1 (Pyridoxal phosphate phosphatase-related protein) [NCBI Gene 838347] {aka Arabidopsis thaliana phosphoethanolamine/phosphocholine phosphatase 1, AtPEPC1, F11A6.5, F11A6_5, phosphoethanolamine/phosphocholine phosphatase 1}, GL3 (basic helix-loop-helix (bHLH) DNA-binding superfamily protein) [NCBI Gene 834133] {aka GLABRA 3, GLABROUS 3, MYC6.2}, JKD (C2H2-like zinc finger protein) [NCBI Gene 831919] {aka F15A17.180, F15A17_180, JACKDAW}, TRY (Homeodomain-like superfamily protein) [NCBI Gene 835401] {aka MFH8.14, MFH8_14, TRIPTYCHON}, RHS12 (root hair specific 12) [NCBI Gene 820240] {aka root hair specific 12}, ZIP9 (ZIP metal ion transporter family) [NCBI Gene 829439] {aka ATZIP9, F4I10.1}, CPL3 (CAPRICE-like MYB3) [NCBI Gene 827917] {aka CAPRICE-like MYB3, ENHANCER OF TRY AND CPC 3, ETC3, F2N1.40, F2N1_40}, SPX3 (SPX domain protein 3) [NCBI Gene 819120] {aka ARABIDOPSIS THALIANA SPX DOMAIN GENE 3, ATSPX3, SPX domain gene 3, T14P1.6}, PAP23 (purple acid phosphatase 23) [NCBI Gene 827004] {aka ATPAP23, F18A5.90, F18A5_90, purple acid phosphatase 23}, MT2A (metallothionein 2A) [NCBI Gene 820098] {aka ARABIDOPSIS THALIANA METALLOTHIONEIN-1, ARABIDOPSIS THALIANA METALLOTHIONEIN-K, ATMT-1, ATMT-K, metallothionein 2A}, RHS16 (root hair specific 16) [NCBI Gene 829039] {aka F19B15.210, F19B15_210, root hair specific 16}, IRT3 (iron regulated transporter 3) [NCBI Gene 842387] {aka ATIRT3, IRON REGULATED TRANSPORTER 3, T7P1.10, T7P1_10, iron regulated transporter 3}, RHD1 (NAD(P)-binding Rossmann-fold superfamily protein) [NCBI Gene 842752] {aka F15H21.11, F15H21_11, REB1, ROOT EPIDERMAL BULGER1, ROOT HAIR DEFECTIVE 1, UDP-GLUCOSE 4-EPIMERASE}, AT2G30670 (NAD(P)-binding Rossmann-fold superfamily protein) [NCBI Gene 817617] {aka T11J7.6, T11J7_6}, MOP10 (Pollen Ole e 1 allergen and extensin family protein) [NCBI Gene 830433] {aka AtPRPL1, MOP10.4, MOP10_4, PRPL1, proline-rich protein-like 1}, PLP6 (PATATIN-like protein 6) [NCBI Gene 818507] {aka PATATIN-like protein 6, PLA IIB, T16B24.14, T16B24_14}, ASY1 (DNA-binding HORMA family protein) [NCBI Gene 843058] {aka ASYNAPTIC 1, ATASY1, F1N21.19}, MYB23 (myb domain protein 23) [NCBI Gene 834031] {aka ATMYB23, ATMYBRTF, MPO12.40, MPO12_40, MYB DOMAIN PROTEIN 23, myb domain protein 23}, PRP3 (proline-rich protein 3) [NCBI Gene 825442] {aka ARABIDOPSIS THALIANA PROLINE-RICH PROTEIN 3, ATPRP3, proline-rich protein 3}, GDPD5 (PLC-like phosphodiesterases superfamily protein) [NCBI Gene 843761] {aka AtGDPD5, F1O17.12, F1O17_12, glycerophosphodiester phosphodiesterase 5}, AT4G08410 (Proline-rich extensin-like family protein) [NCBI Gene 826400] {aka T28D5.100, T28D5_100}, CPC (Homeodomain-like superfamily protein) [NCBI Gene 819249] {aka CAPRICE, F11C10.10, MYB FAMILY TRANSCRIPTION FACTOR CPC}, AT5G20790 (uncharacterized protein) [NCBI Gene 832202] {aka T1M15.190, T1M15_190}, PLPB (PAS/LOV protein B) [NCBI Gene 814800] {aka PAS/LOV PROTEIN, PAS/LOV PROTEIN A, PAS/LOV PROTEIN C, PAS/LOV protein B, PLP, PLPA}, PLDP2 (phospholipase D P2) [NCBI Gene 819730] {aka F18C1.10, F18C1_10, PDLZ2, PHOSPHOLIPASE D, PHOSPHOLIPASE D ZETA 2, PLDZETA2}, PHT1;7 (phosphate transporter 1;7) [NCBI Gene 824635] {aka phosphate transporter 1;7}, AT5G42050 (DCD (Development and Cell Death) domain protein) [NCBI Gene 834210] {aka MJC20.15, MJC20_15}, PS2 (inorganic pyrophosphatase 1) [NCBI Gene 843632] {aka ATPS2, AtPPsPase1, F3N23.21, F3N23_21, PPsPase1, phosphate starvation-induced gene 2}, PCR2 (PLANT CADMIUM RESISTANCE 2) [NCBI Gene 838052] {aka AtPCR2, F10B6.27, F10B6_27, PLANT CADMIUM RESISTANCE 2}, XTH14 (xyloglucan endotransglucosylase/hydrolase 14) [NCBI Gene 828687] {aka ATXTH14, F14M19.100, F14M19_100, XTR9, xyloglucan endotransglucosylase/hydrolase 14, xyloglucan endotransglycosylase 9}, DRP4D (miscRNA) [NCBI Gene 3767584] {aka Dynamin related protein 4D, F8A5.6}, TTG1 (Transducin/WD40 repeat-like superfamily protein) [NCBI Gene 832523] {aka ATTTG1, K18P6.4, K18P6_4, TRANSPARENT TESTA GLABRA 1, TTG, UNARMED 23}, AT1G15670 (Galactose oxidase/kelch repeat superfamily protein) [NCBI Gene 838136] {aka F7H2.1, F7H2_1, KFB01, KISS ME DEADLY 2, KMD2, Kelch repeat F-box 1}, AT5G40153 (peroxidase) [NCBI Gene 28721236], AT3G49960 (Peroxidase superfamily protein) [NCBI Gene 824158], AT1G30870 (Peroxidase superfamily protein) [NCBI Gene 839971] {aka T17H7.19}, PRXCB (peroxidase CB) [NCBI Gene 824073] {aka ARABIDOPSIS THALIANA PEROXIDASE CB, ATPCB, ATPERX34, F2K15.3, PEROXIDASE 34, PERX34}, PLP4 (PATATIN-like protein 4) [NCBI Gene 829859] {aka AP22.16, AP22_16, AtPLAIVC, PATATIN-like protein 4, PLA V, PLAIII{beta}}, HA7 (H[+]-ATPase 7) [NCBI Gene 825204] {aka AHA7, H(+)-ATPase 7, T8B10.1}, AT5G49870 (Mannose-binding lectin superfamily protein) [NCBI Gene 835050] {aka K9P8.1, K9P8_1}, GRF11 (general regulatory factor 11) [NCBI Gene 840380] {aka 14-3-3 PROTEIN GF14OMICRON, F11O6.13, GF14 OMICRON, RHS5, ROOT HAIR SPECIFIC 5, general regulatory factor 11}, AT2G38250 (Homeodomain-like superfamily protein) [NCBI Gene 818404] {aka F16M14.18, F16M14_18}, WRKY75 (WRKY DNA-binding protein 75) [NCBI Gene 831147] {aka ARABIDOPSIS THALIANA WRKY DNA-BINDING PROTEIN 75, ATWRKY75, T19L5.40, T19L5_40, WRKY DNA-binding protein 75}, PER1 (1-cysteine peroxiredoxin 1) [NCBI Gene 841231] {aka 1-CYS PEROXIREDOXIN, 1-cysteine peroxiredoxin 1, ATPER1, F21D18.15, F21D18_15}, SQD2 (sulfoquinovosyldiacylglycerol 2) [NCBI Gene 831888] {aka F7J8.200, F7J8_200, SULFOLIPID SYNTHASE, sulfoquinovosyldiacylglycerol 2}, EGL3 (basic helix-loop-helix (bHLH) DNA-binding superfamily protein) [NCBI Gene 842669] {aka ATMYC-2, AtEGL3, EGL1, ENHANCER OF GLABRA 3, F24D7.16, F24D7_16}, LRX2 (leucine-rich repeat/extensin 2) [NCBI Gene 842542] {aka F24O1.19, leucine-rich repeat/extensin 2}
- **Diseases:** hypoxia (MESH:D000860), Pi deficiency (MESH:D007153)
- **Chemicals:** ethylene (MESH:C036216), G3P (MESH:C029620), DAG (MESH:D004075), P-Cho (MESH:C043572), cytokinin (MESH:D003583), auxin (MESH:D007210), Phosphate (MESH:D010710), lipid (MESH:D008055), P (MESH:D010758), sugar (MESH:D000073893), LPC (MESH:D008244), phytate (MESH:D010833), DGDG (MESH:C007388), Technovit 7100 (MESH:C053012), ethanol (MESH:D000431), PE (MESH:C483858), SYBR Green (MESH:C098022), Cho (MESH:C034482), membrane lipid (MESH:D008563), sulfolipid (MESH:C015518), KCl (MESH:D011189), PI (MESH:D011419), manganese (MESH:D008345), PCho (MESH:D010767), PLs (MESH:D010743), PC (MESH:D010713), NaOCl (MESH:D012973), potassium (MESH:D011188), Fe (MESH:D007501), Zn (MESH:D015032), Pi (MESH:D010716), Fe2+ (-), jasmonate (MESH:C011006), Inositol (MESH:D007294), PA (MESH:D010712), water (MESH:D014867)
- **Species:** Arabidopsis thaliana (mouse-ear cress, species) [taxon 3702]
- **Mutations:** C1C, serine/threonine
- **Cell lines:** S2 — Drosophila melanogaster (Fruit fly), Spontaneously immortalized cell line (CVCL_Z232)

## Full text

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## Figures

7 figures with captions in the complete paper: https://tomesphere.com/paper/PMC4507782/full.md

## References

76 references — full list in the complete paper: https://tomesphere.com/paper/PMC4507782/full.md

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Source: https://tomesphere.com/paper/PMC4507782