PPP1, a plant-specific regulator of transcription controls Arabidopsis development and PIN expression

René Benjamins; Elke Barbez; Martina Ortbauer; Inez Terpstra; Doris Lucyshyn; Jeanette Moulinier-Anzola; Muhammad Asaf Khan; Johannes Leitner; Nenad Malenica; Haroon Butt; Barbara Korbei; Ben Scheres; Jürgen Kleine-Vehn; Christian Luschnig

doi:10.1038/srep32196

PPP1, a plant-specific regulator of transcription controls Arabidopsis development and PIN expression

René Benjamins^*, Elke Barbez, Martina Ortbauer, Inez Terpstra, Doris Lucyshyn, Jeanette Moulinier-Anzola, Muhammad Asaf Khan, Johannes Leitner, Nenad Malenica, Haroon Butt, Barbara Korbei, Ben Scheres, Jürgen Kleine-Vehn, Christian Luschnig

^*Corresponding author for this work

Biological, Environmental Sciences and Engineering

Research output: Contribution to journal › Article › peer-review

6 Scopus citations

Abstract

Directional transport of auxin is essential for plant development, with PIN auxin transport proteins representing an integral part of the machinery that controls hormone distribution. However, unlike the rapidly emerging framework of molecular determinants regulating PIN protein abundance and subcellular localization, insights into mechanisms controlling PIN transcription are still limited. Here we describe PIN2 PROMOTER BINDING PROTEIN 1 (PPP1), an evolutionary conserved plant-specific DNA binding protein that acts on transcription of PIN genes. Consistent with PPP1 DNA-binding activity, PPP1 reporter proteins are nuclear localized and analysis of PPP1 null alleles and knockdown lines indicated a function as a positive regulator of PIN expression. Furthermore, we show that ppp1 pleiotropic mutant phenotypes are partially reverted by PIN overexpression, and results are presented that underline a role of PPP1-PIN promoter interaction in PIN expression control. Collectively, our findings identify an elementary, thus far unknown, plant-specific DNA-binding protein required for post-embryonic plant development, in general, and correct expression of PIN genes, in particular.

Original language	English (US)
Article number	32196
Journal	Scientific Reports
Volume	6
DOIs	https://doi.org/10.1038/srep32196
State	Published - Aug 24 2016

Bibliographical note

Funding Information:
The authors acknowledge research funding by the FWF (Austrian Science Fund, P19585; P25931) to C.L. and (P26568-B16; P26591-B16) to J.K.V, the WWTF (Vienna Science and Technology Fund, Vienna Research Group) to J.K.V, the ERC (European Research Council, Starting Grant 639478-AuxinER) to J.K-V, as well as a VENI fellowship to R.B. by NWO (Netherlands Organization for Scientific Research). We thank Pieter Ouwerkerk for providing the yeast one-hybrid system, Bert van der Zaal for cDNA library stocks, Marie-Theres Hauser for an Arabidopsis cosmid library and suggestions on phylogenetic analysis, NASC for seed stocks, and David Jackson for providing the DR5::mRFP construct. CYCB1;1:GUS was provided by John Celenza. We acknowledge Ikram Blilou, Dong Ping Bao, Sonja Graner and Herman van der Klis for technical support and Frits Kindt and Ronald Leito for artwork. We wish to thank Joseph Strauss for support in setting up EMSA, and Robert Konrat for support with the protein meta-structure analysis.

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Benjamins, R., Barbez, E., Ortbauer, M., Terpstra, I., Lucyshyn, D., Moulinier-Anzola, J., Khan, M. A., Leitner, J., Malenica, N., Butt, H., Korbei, B., Scheres, B., Kleine-Vehn, J., & Luschnig, C. (2016). PPP1, a plant-specific regulator of transcription controls Arabidopsis development and PIN expression. Scientific Reports, 6, Article 32196. https://doi.org/10.1038/srep32196

@article{c94b6524ef3347deba61134d25dbfb05,

title = "PPP1, a plant-specific regulator of transcription controls Arabidopsis development and PIN expression",

abstract = "Directional transport of auxin is essential for plant development, with PIN auxin transport proteins representing an integral part of the machinery that controls hormone distribution. However, unlike the rapidly emerging framework of molecular determinants regulating PIN protein abundance and subcellular localization, insights into mechanisms controlling PIN transcription are still limited. Here we describe PIN2 PROMOTER BINDING PROTEIN 1 (PPP1), an evolutionary conserved plant-specific DNA binding protein that acts on transcription of PIN genes. Consistent with PPP1 DNA-binding activity, PPP1 reporter proteins are nuclear localized and analysis of PPP1 null alleles and knockdown lines indicated a function as a positive regulator of PIN expression. Furthermore, we show that ppp1 pleiotropic mutant phenotypes are partially reverted by PIN overexpression, and results are presented that underline a role of PPP1-PIN promoter interaction in PIN expression control. Collectively, our findings identify an elementary, thus far unknown, plant-specific DNA-binding protein required for post-embryonic plant development, in general, and correct expression of PIN genes, in particular.",

author = "Ren{\'e} Benjamins and Elke Barbez and Martina Ortbauer and Inez Terpstra and Doris Lucyshyn and Jeanette Moulinier-Anzola and Khan, {Muhammad Asaf} and Johannes Leitner and Nenad Malenica and Haroon Butt and Barbara Korbei and Ben Scheres and J{\"u}rgen Kleine-Vehn and Christian Luschnig",

note = "Funding Information: The authors acknowledge research funding by the FWF (Austrian Science Fund, P19585; P25931) to C.L. and (P26568-B16; P26591-B16) to J.K.V, the WWTF (Vienna Science and Technology Fund, Vienna Research Group) to J.K.V, the ERC (European Research Council, Starting Grant 639478-AuxinER) to J.K-V, as well as a VENI fellowship to R.B. by NWO (Netherlands Organization for Scientific Research). We thank Pieter Ouwerkerk for providing the yeast one-hybrid system, Bert van der Zaal for cDNA library stocks, Marie-Theres Hauser for an Arabidopsis cosmid library and suggestions on phylogenetic analysis, NASC for seed stocks, and David Jackson for providing the DR5::mRFP construct. CYCB1;1:GUS was provided by John Celenza. We acknowledge Ikram Blilou, Dong Ping Bao, Sonja Graner and Herman van der Klis for technical support and Frits Kindt and Ronald Leito for artwork. We wish to thank Joseph Strauss for support in setting up EMSA, and Robert Konrat for support with the protein meta-structure analysis.",

year = "2016",

month = aug,

day = "24",

doi = "10.1038/srep32196",

language = "English (US)",

volume = "6",

journal = "Scientific Reports",

issn = "2045-2322",

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T1 - PPP1, a plant-specific regulator of transcription controls Arabidopsis development and PIN expression

AU - Benjamins, René

AU - Barbez, Elke

AU - Ortbauer, Martina

AU - Terpstra, Inez

AU - Lucyshyn, Doris

AU - Moulinier-Anzola, Jeanette

AU - Khan, Muhammad Asaf

AU - Leitner, Johannes

AU - Malenica, Nenad

AU - Butt, Haroon

AU - Korbei, Barbara

AU - Scheres, Ben

AU - Kleine-Vehn, Jürgen

AU - Luschnig, Christian

N1 - Funding Information: The authors acknowledge research funding by the FWF (Austrian Science Fund, P19585; P25931) to C.L. and (P26568-B16; P26591-B16) to J.K.V, the WWTF (Vienna Science and Technology Fund, Vienna Research Group) to J.K.V, the ERC (European Research Council, Starting Grant 639478-AuxinER) to J.K-V, as well as a VENI fellowship to R.B. by NWO (Netherlands Organization for Scientific Research). We thank Pieter Ouwerkerk for providing the yeast one-hybrid system, Bert van der Zaal for cDNA library stocks, Marie-Theres Hauser for an Arabidopsis cosmid library and suggestions on phylogenetic analysis, NASC for seed stocks, and David Jackson for providing the DR5::mRFP construct. CYCB1;1:GUS was provided by John Celenza. We acknowledge Ikram Blilou, Dong Ping Bao, Sonja Graner and Herman van der Klis for technical support and Frits Kindt and Ronald Leito for artwork. We wish to thank Joseph Strauss for support in setting up EMSA, and Robert Konrat for support with the protein meta-structure analysis.

PY - 2016/8/24

Y1 - 2016/8/24

N2 - Directional transport of auxin is essential for plant development, with PIN auxin transport proteins representing an integral part of the machinery that controls hormone distribution. However, unlike the rapidly emerging framework of molecular determinants regulating PIN protein abundance and subcellular localization, insights into mechanisms controlling PIN transcription are still limited. Here we describe PIN2 PROMOTER BINDING PROTEIN 1 (PPP1), an evolutionary conserved plant-specific DNA binding protein that acts on transcription of PIN genes. Consistent with PPP1 DNA-binding activity, PPP1 reporter proteins are nuclear localized and analysis of PPP1 null alleles and knockdown lines indicated a function as a positive regulator of PIN expression. Furthermore, we show that ppp1 pleiotropic mutant phenotypes are partially reverted by PIN overexpression, and results are presented that underline a role of PPP1-PIN promoter interaction in PIN expression control. Collectively, our findings identify an elementary, thus far unknown, plant-specific DNA-binding protein required for post-embryonic plant development, in general, and correct expression of PIN genes, in particular.

AB - Directional transport of auxin is essential for plant development, with PIN auxin transport proteins representing an integral part of the machinery that controls hormone distribution. However, unlike the rapidly emerging framework of molecular determinants regulating PIN protein abundance and subcellular localization, insights into mechanisms controlling PIN transcription are still limited. Here we describe PIN2 PROMOTER BINDING PROTEIN 1 (PPP1), an evolutionary conserved plant-specific DNA binding protein that acts on transcription of PIN genes. Consistent with PPP1 DNA-binding activity, PPP1 reporter proteins are nuclear localized and analysis of PPP1 null alleles and knockdown lines indicated a function as a positive regulator of PIN expression. Furthermore, we show that ppp1 pleiotropic mutant phenotypes are partially reverted by PIN overexpression, and results are presented that underline a role of PPP1-PIN promoter interaction in PIN expression control. Collectively, our findings identify an elementary, thus far unknown, plant-specific DNA-binding protein required for post-embryonic plant development, in general, and correct expression of PIN genes, in particular.

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DO - 10.1038/srep32196

M3 - Article

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AN - SCOPUS:84984677236

SN - 2045-2322

VL - 6

JO - Scientific Reports

JF - Scientific Reports

M1 - 32196

ER -

PPP1, a plant-specific regulator of transcription controls Arabidopsis development and PIN expression

Abstract

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