Arabidopsis PLETHORA transcription factors control phyllotaxis

Kalika Prasad; Stephen P. Grigg; Michalis Barkoulas; Ram Kishor Yadav; Gabino F. Sanchez-Perez; Violaine Pinon; Ikram Blilou; Hugo Hofhuis; Pankaj Dhonukshe; Carla Galinha; Ari Pekka Mähönen; Wally H. Muller; Smita Raman; Arie J. Verkleij; Berend Snel; G. Venugopala Reddy; Miltos Tsiantis; Ben Scheres

doi:10.1016/j.cub.2011.05.009

Arabidopsis PLETHORA transcription factors control phyllotaxis

Kalika Prasad, Stephen P. Grigg, Michalis Barkoulas, Ram Kishor Yadav, Gabino F. Sanchez-Perez, Violaine Pinon, Ikram Blilou, Hugo Hofhuis, Pankaj Dhonukshe, Carla Galinha, Ari Pekka Mähönen, Wally H. Muller, Smita Raman, Arie J. Verkleij, Berend Snel, G. Venugopala Reddy, Miltos Tsiantis, Ben Scheres^*

^*Corresponding author for this work

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

116 Scopus citations

Abstract

The pattern of plant organ initiation at the shoot apical meristem (SAM), termed phyllotaxis, displays regularities that have long intrigued botanists and mathematicians alike. In the SAM, the central zone (CZ) contains a population of stem cells that replenish the surrounding peripheral zone (PZ), where organs are generated in regular patterns. These patterns differ between species and may change in response to developmental or environmental cues [1]. Expression analysis of auxin efflux facilitators of the PIN-FORMED (PIN) family combined with modeling of auxin transport has indicated that organ initiation is associated with intracellular polarization of PIN proteins and auxin accumulation [2-10]. However, regulators that modulate PIN activity to determine phyllotactic patterns have hitherto been unknown. Here we reveal that three redundantly acting PLETHORA (PLT)-like AP2 domain transcription factors control shoot organ positioning in the model plant Arabidopsis thaliana. Loss of PLT3, PLT5, and PLT7 function leads to nonrandom, metastable changes in phyllotaxis. Phyllotactic changes in plt3plt5plt7 mutants are largely attributable to misregulation of PIN1 and can be recapitulated by reducing PIN1 dosage, revealing that PLT proteins are key regulators of PIN1 activity in control of phyllotaxis.

Original language	English (US)
Pages (from-to)	1123-1128
Number of pages	6
Journal	Current Biology
Volume	21
Issue number	13
DOIs	https://doi.org/10.1016/j.cub.2011.05.009
State	Published - Jul 12 2011
Externally published	Yes

ASJC Scopus subject areas

General Biochemistry, Genetics and Molecular Biology
General Agricultural and Biological Sciences

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10.1016/j.cub.2011.05.009

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Prasad, K., Grigg, S. P., Barkoulas, M., Yadav, R. K., Sanchez-Perez, G. F., Pinon, V., Blilou, I., Hofhuis, H., Dhonukshe, P., Galinha, C., Mähönen, A. P., Muller, W. H., Raman, S., Verkleij, A. J., Snel, B., Reddy, G. V., Tsiantis, M., & Scheres, B. (2011). Arabidopsis PLETHORA transcription factors control phyllotaxis. Current Biology, 21(13), 1123-1128. https://doi.org/10.1016/j.cub.2011.05.009

@article{aba2d176562c4970aae2d342aaea7bc6,

title = "Arabidopsis PLETHORA transcription factors control phyllotaxis",

abstract = "The pattern of plant organ initiation at the shoot apical meristem (SAM), termed phyllotaxis, displays regularities that have long intrigued botanists and mathematicians alike. In the SAM, the central zone (CZ) contains a population of stem cells that replenish the surrounding peripheral zone (PZ), where organs are generated in regular patterns. These patterns differ between species and may change in response to developmental or environmental cues [1]. Expression analysis of auxin efflux facilitators of the PIN-FORMED (PIN) family combined with modeling of auxin transport has indicated that organ initiation is associated with intracellular polarization of PIN proteins and auxin accumulation [2-10]. However, regulators that modulate PIN activity to determine phyllotactic patterns have hitherto been unknown. Here we reveal that three redundantly acting PLETHORA (PLT)-like AP2 domain transcription factors control shoot organ positioning in the model plant Arabidopsis thaliana. Loss of PLT3, PLT5, and PLT7 function leads to nonrandom, metastable changes in phyllotaxis. Phyllotactic changes in plt3plt5plt7 mutants are largely attributable to misregulation of PIN1 and can be recapitulated by reducing PIN1 dosage, revealing that PLT proteins are key regulators of PIN1 activity in control of phyllotaxis.",

author = "Kalika Prasad and Grigg, {Stephen P.} and Michalis Barkoulas and Yadav, {Ram Kishor} and Sanchez-Perez, {Gabino F.} and Violaine Pinon and Ikram Blilou and Hugo Hofhuis and Pankaj Dhonukshe and Carla Galinha and M{\"a}h{\"o}nen, {Ari Pekka} and Muller, {Wally H.} and Smita Raman and Verkleij, {Arie J.} and Berend Snel and Reddy, {G. Venugopala} and Miltos Tsiantis and Ben Scheres",

note = "Funding Information: K.P. was funded by a long-term European Molecular Biology Organization fellowship and by Netherlands Organisation for Scientific Research (NWO) Spinoza and European Research Council advanced investigator grants. G.F.S.-P. was funded by a CBSG2/NCSB grant. Support from NWO-VENI to P.D., NWO-VIDI to I.B., and a Human Frontier Science Program fellowship to A.P.M. is acknowledged. H.H. was funded by NWO-ALW. Work in M.T.{\textquoteright}s laboratory was funded by the Biotechnology and Biological Sciences Research Council (BB/F012934/1), the Gatsby Charitable Foundation, and the Royal Society. Live-imaging data were generated by the Microscopy Core at the Institute for Integrative Genome Biology at the University of California, Riverside and were funded by National Science Foundation grant IOS-0718046 to G.V.R. ",

year = "2011",

month = jul,

day = "12",

doi = "10.1016/j.cub.2011.05.009",

language = "English (US)",

volume = "21",

pages = "1123--1128",

journal = "Current Biology",

issn = "0960-9822",

publisher = "Elsevier",

number = "13",

}

Prasad, K, Grigg, SP, Barkoulas, M, Yadav, RK, Sanchez-Perez, GF, Pinon, V, Blilou, I, Hofhuis, H, Dhonukshe, P, Galinha, C, Mähönen, AP, Muller, WH, Raman, S, Verkleij, AJ, Snel, B, Reddy, GV, Tsiantis, M & Scheres, B 2011, 'Arabidopsis PLETHORA transcription factors control phyllotaxis', Current Biology, vol. 21, no. 13, pp. 1123-1128. https://doi.org/10.1016/j.cub.2011.05.009

TY - JOUR

T1 - Arabidopsis PLETHORA transcription factors control phyllotaxis

AU - Prasad, Kalika

AU - Grigg, Stephen P.

AU - Barkoulas, Michalis

AU - Yadav, Ram Kishor

AU - Sanchez-Perez, Gabino F.

AU - Pinon, Violaine

AU - Blilou, Ikram

AU - Hofhuis, Hugo

AU - Dhonukshe, Pankaj

AU - Galinha, Carla

AU - Mähönen, Ari Pekka

AU - Muller, Wally H.

AU - Raman, Smita

AU - Verkleij, Arie J.

AU - Snel, Berend

AU - Reddy, G. Venugopala

AU - Tsiantis, Miltos

AU - Scheres, Ben

N1 - Funding Information: K.P. was funded by a long-term European Molecular Biology Organization fellowship and by Netherlands Organisation for Scientific Research (NWO) Spinoza and European Research Council advanced investigator grants. G.F.S.-P. was funded by a CBSG2/NCSB grant. Support from NWO-VENI to P.D., NWO-VIDI to I.B., and a Human Frontier Science Program fellowship to A.P.M. is acknowledged. H.H. was funded by NWO-ALW. Work in M.T.’s laboratory was funded by the Biotechnology and Biological Sciences Research Council (BB/F012934/1), the Gatsby Charitable Foundation, and the Royal Society. Live-imaging data were generated by the Microscopy Core at the Institute for Integrative Genome Biology at the University of California, Riverside and were funded by National Science Foundation grant IOS-0718046 to G.V.R.

PY - 2011/7/12

Y1 - 2011/7/12

N2 - The pattern of plant organ initiation at the shoot apical meristem (SAM), termed phyllotaxis, displays regularities that have long intrigued botanists and mathematicians alike. In the SAM, the central zone (CZ) contains a population of stem cells that replenish the surrounding peripheral zone (PZ), where organs are generated in regular patterns. These patterns differ between species and may change in response to developmental or environmental cues [1]. Expression analysis of auxin efflux facilitators of the PIN-FORMED (PIN) family combined with modeling of auxin transport has indicated that organ initiation is associated with intracellular polarization of PIN proteins and auxin accumulation [2-10]. However, regulators that modulate PIN activity to determine phyllotactic patterns have hitherto been unknown. Here we reveal that three redundantly acting PLETHORA (PLT)-like AP2 domain transcription factors control shoot organ positioning in the model plant Arabidopsis thaliana. Loss of PLT3, PLT5, and PLT7 function leads to nonrandom, metastable changes in phyllotaxis. Phyllotactic changes in plt3plt5plt7 mutants are largely attributable to misregulation of PIN1 and can be recapitulated by reducing PIN1 dosage, revealing that PLT proteins are key regulators of PIN1 activity in control of phyllotaxis.

AB - The pattern of plant organ initiation at the shoot apical meristem (SAM), termed phyllotaxis, displays regularities that have long intrigued botanists and mathematicians alike. In the SAM, the central zone (CZ) contains a population of stem cells that replenish the surrounding peripheral zone (PZ), where organs are generated in regular patterns. These patterns differ between species and may change in response to developmental or environmental cues [1]. Expression analysis of auxin efflux facilitators of the PIN-FORMED (PIN) family combined with modeling of auxin transport has indicated that organ initiation is associated with intracellular polarization of PIN proteins and auxin accumulation [2-10]. However, regulators that modulate PIN activity to determine phyllotactic patterns have hitherto been unknown. Here we reveal that three redundantly acting PLETHORA (PLT)-like AP2 domain transcription factors control shoot organ positioning in the model plant Arabidopsis thaliana. Loss of PLT3, PLT5, and PLT7 function leads to nonrandom, metastable changes in phyllotaxis. Phyllotactic changes in plt3plt5plt7 mutants are largely attributable to misregulation of PIN1 and can be recapitulated by reducing PIN1 dosage, revealing that PLT proteins are key regulators of PIN1 activity in control of phyllotaxis.

UR - http://www.scopus.com/inward/record.url?scp=79960181663&partnerID=8YFLogxK

U2 - 10.1016/j.cub.2011.05.009

DO - 10.1016/j.cub.2011.05.009

M3 - Article

C2 - 21700457

AN - SCOPUS:79960181663

SN - 0960-9822

VL - 21

SP - 1123

EP - 1128

JO - Current Biology

JF - Current Biology

IS - 13

ER -

Arabidopsis PLETHORA transcription factors control phyllotaxis

Abstract

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