A coherent feed-forward loop drives vascular regeneration in damaged aerial organs of plants growing in a normal developmental context

Dhanya Radhakrishnan; Anju Pallipurath Shanmukhan; Abdul Kareem; Mohammed Aiyaz; Vijina Varapparambathu; Ashna Toms; Merijn Kerstens; Devisree Valsakumar; Amit N. Landge; Anil Shaji; Mathew K. Mathew; Megan G. Sawchuk; Enrico Scarpella; Beth A. Krizek; Idan Efroni; Ari Pekka Mähönen; Viola Willemsen; Ben Scheres; Kalika Prasad

doi:10.1242/dev.185710

A coherent feed-forward loop drives vascular regeneration in damaged aerial organs of plants growing in a normal developmental context

Dhanya Radhakrishnan, Anju Pallipurath Shanmukhan, Abdul Kareem, Mohammed Aiyaz, Vijina Varapparambathu, Ashna Toms, Merijn Kerstens, Devisree Valsakumar, Amit N. Landge, Anil Shaji, Mathew K. Mathew, Megan G. Sawchuk, Enrico Scarpella, Beth A. Krizek, Idan Efroni, Ari Pekka Mähönen, Viola Willemsen, Ben Scheres, Kalika Prasad^*

^*Corresponding author for this work

Institute of Plant Sciences and Genetics in Agriculture

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

17 Scopus citations

Abstract

Aerial organs of plants, being highly prone to local injuries, require tissue restoration to ensure their survival. However, knowledge of the underlying mechanism is sparse. In this study, we mimicked natural injuries in growing leaves and stems to study the reunion between mechanically disconnected tissues. We show that PLETHORA (PLT) and AINTEGUMENTA (ANT) genes, which encode stem cell-promoting factors, are activated and contribute to vascular regeneration in response to these injuries. PLT proteins bind to and activate the CUC2 promoter. PLT proteins and CUC2 regulate the transcription of the local auxin biosynthesis gene YUC4 in a coherent feed-forward loop, and this process is necessary to drive vascular regeneration. In the absence of this PLT-mediated regeneration response, leaf ground tissue cells can neither acquire the early vascular identity marker ATHB8, nor properly polarise auxin transporters to specify new venation paths. The PLT-CUC2 module is required for vascular regeneration, but is dispensable for midvein formation in leaves. We reveal the mechanisms of vascular regeneration in plants and distinguish between the wound-repair ability of the tissue and its formation during normal development.

Original language	American English
Article number	185710
Journal	Development (Cambridge)
Volume	147
Issue number	6
DOIs	https://doi.org/10.1242/dev.185710
State	Published - 30 Mar 2020

Bibliographical note

Funding Information:
K.P. acknowledges grants from the Department of Biotechnology (DBT), Government of India [grant BT/PR12394/AGIII/103/891/2014] and Department of Science and Technology, Science and Engineering Research Board (DST-SERB), Government of India [grant EMR/2017/002503/PS] and also acknowledges the Indian Institute of Science Education and Research Thiruvananthapuram (IISER-TVM) for infrastructure and financial support. D.R. acknowledges a University Grants Commission (UGC) fellowship. A.P.S., V.V. and A.T. are recipients of Council of Scientific and Industrial Research (CSIR) fellowships. A.K. was supported by an Indian Institute of Science Education and Research-Thiruvananthapuram fellowship. M.A. acknowledges Department of Biotechnology (DBT), Ministry of Science and Technology, Government of India for granting the DBT-Post Doctoral Fellowship (DBT-RA Program). D.V. was a recipient of an Innovation in Science Pursuit for Inspired Research scholarship, and A.N.L was supported by a Kishore Vaigyanik Protsahan Yojana scholarship of the Department of Science and Technology, Government of India. A.P.M. acknowledges grants from the Academy of Finland [grants 266431 and 271832]. I.E. acknowledges the Israel Science Foundation [ISF966/17] and the Howard Hughes Medical Institute [International Research Scholar Grant 55008730]. B.A.K. was supported by a grant from National Science Foundation (NSF) [grant NSFIOS135442]. E.S. was supported by Discovery Grants of the Natural Science and Engineering Research Council of Canada [grants NSERC RGPIN-2016-04736 and NSERC RGPAS 492872-2016].

Publisher Copyright:
© 2020 Company of Biologists Ltd. All rights reserved.

Keywords

Arabidopsis
Auxin
CUC2
PIN1
PLT
Vascular regeneration
Wound repair

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Radhakrishnan, D., Shanmukhan, A. P., Kareem, A., Aiyaz, M., Varapparambathu, V., Toms, A., Kerstens, M., Valsakumar, D., Landge, A. N., Shaji, A., Mathew, M. K., Sawchuk, M. G., Scarpella, E., Krizek, B. A., Efroni, I., Mähönen, A. P., Willemsen, V., Scheres, B., & Prasad, K. (2020). A coherent feed-forward loop drives vascular regeneration in damaged aerial organs of plants growing in a normal developmental context. Development (Cambridge), 147(6), Article 185710. https://doi.org/10.1242/dev.185710

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title = "A coherent feed-forward loop drives vascular regeneration in damaged aerial organs of plants growing in a normal developmental context",

abstract = "Aerial organs of plants, being highly prone to local injuries, require tissue restoration to ensure their survival. However, knowledge of the underlying mechanism is sparse. In this study, we mimicked natural injuries in growing leaves and stems to study the reunion between mechanically disconnected tissues. We show that PLETHORA (PLT) and AINTEGUMENTA (ANT) genes, which encode stem cell-promoting factors, are activated and contribute to vascular regeneration in response to these injuries. PLT proteins bind to and activate the CUC2 promoter. PLT proteins and CUC2 regulate the transcription of the local auxin biosynthesis gene YUC4 in a coherent feed-forward loop, and this process is necessary to drive vascular regeneration. In the absence of this PLT-mediated regeneration response, leaf ground tissue cells can neither acquire the early vascular identity marker ATHB8, nor properly polarise auxin transporters to specify new venation paths. The PLT-CUC2 module is required for vascular regeneration, but is dispensable for midvein formation in leaves. We reveal the mechanisms of vascular regeneration in plants and distinguish between the wound-repair ability of the tissue and its formation during normal development.",

keywords = "Arabidopsis, Auxin, CUC2, PIN1, PLT, Vascular regeneration, Wound repair",

author = "Dhanya Radhakrishnan and Shanmukhan, {Anju Pallipurath} and Abdul Kareem and Mohammed Aiyaz and Vijina Varapparambathu and Ashna Toms and Merijn Kerstens and Devisree Valsakumar and Landge, {Amit N.} and Anil Shaji and Mathew, {Mathew K.} and Sawchuk, {Megan G.} and Enrico Scarpella and Krizek, {Beth A.} and Idan Efroni and M{\"a}h{\"o}nen, {Ari Pekka} and Viola Willemsen and Ben Scheres and Kalika Prasad",

note = "Funding Information: K.P. acknowledges grants from the Department of Biotechnology (DBT), Government of India [grant BT/PR12394/AGIII/103/891/2014] and Department of Science and Technology, Science and Engineering Research Board (DST-SERB), Government of India [grant EMR/2017/002503/PS] and also acknowledges the Indian Institute of Science Education and Research Thiruvananthapuram (IISER-TVM) for infrastructure and financial support. D.R. acknowledges a University Grants Commission (UGC) fellowship. A.P.S., V.V. and A.T. are recipients of Council of Scientific and Industrial Research (CSIR) fellowships. A.K. was supported by an Indian Institute of Science Education and Research-Thiruvananthapuram fellowship. M.A. acknowledges Department of Biotechnology (DBT), Ministry of Science and Technology, Government of India for granting the DBT-Post Doctoral Fellowship (DBT-RA Program). D.V. was a recipient of an Innovation in Science Pursuit for Inspired Research scholarship, and A.N.L was supported by a Kishore Vaigyanik Protsahan Yojana scholarship of the Department of Science and Technology, Government of India. A.P.M. acknowledges grants from the Academy of Finland [grants 266431 and 271832]. I.E. acknowledges the Israel Science Foundation [ISF966/17] and the Howard Hughes Medical Institute [International Research Scholar Grant 55008730]. B.A.K. was supported by a grant from National Science Foundation (NSF) [grant NSFIOS135442]. E.S. was supported by Discovery Grants of the Natural Science and Engineering Research Council of Canada [grants NSERC RGPIN-2016-04736 and NSERC RGPAS 492872-2016]. Publisher Copyright: {\textcopyright} 2020 Company of Biologists Ltd. All rights reserved.",

year = "2020",

month = mar,

day = "30",

doi = "10.1242/dev.185710",

language = "American English",

volume = "147",

journal = "Development (Cambridge)",

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Radhakrishnan, D, Shanmukhan, AP, Kareem, A, Aiyaz, M, Varapparambathu, V, Toms, A, Kerstens, M, Valsakumar, D, Landge, AN, Shaji, A, Mathew, MK, Sawchuk, MG, Scarpella, E, Krizek, BA, Efroni, I, Mähönen, AP, Willemsen, V, Scheres, B & Prasad, K 2020, 'A coherent feed-forward loop drives vascular regeneration in damaged aerial organs of plants growing in a normal developmental context', Development (Cambridge), vol. 147, no. 6, 185710. https://doi.org/10.1242/dev.185710

TY - JOUR

T1 - A coherent feed-forward loop drives vascular regeneration in damaged aerial organs of plants growing in a normal developmental context

AU - Radhakrishnan, Dhanya

AU - Shanmukhan, Anju Pallipurath

AU - Kareem, Abdul

AU - Aiyaz, Mohammed

AU - Varapparambathu, Vijina

AU - Toms, Ashna

AU - Kerstens, Merijn

AU - Valsakumar, Devisree

AU - Landge, Amit N.

AU - Shaji, Anil

AU - Mathew, Mathew K.

AU - Sawchuk, Megan G.

AU - Scarpella, Enrico

AU - Krizek, Beth A.

AU - Efroni, Idan

AU - Mähönen, Ari Pekka

AU - Willemsen, Viola

AU - Scheres, Ben

AU - Prasad, Kalika

N1 - Funding Information: K.P. acknowledges grants from the Department of Biotechnology (DBT), Government of India [grant BT/PR12394/AGIII/103/891/2014] and Department of Science and Technology, Science and Engineering Research Board (DST-SERB), Government of India [grant EMR/2017/002503/PS] and also acknowledges the Indian Institute of Science Education and Research Thiruvananthapuram (IISER-TVM) for infrastructure and financial support. D.R. acknowledges a University Grants Commission (UGC) fellowship. A.P.S., V.V. and A.T. are recipients of Council of Scientific and Industrial Research (CSIR) fellowships. A.K. was supported by an Indian Institute of Science Education and Research-Thiruvananthapuram fellowship. M.A. acknowledges Department of Biotechnology (DBT), Ministry of Science and Technology, Government of India for granting the DBT-Post Doctoral Fellowship (DBT-RA Program). D.V. was a recipient of an Innovation in Science Pursuit for Inspired Research scholarship, and A.N.L was supported by a Kishore Vaigyanik Protsahan Yojana scholarship of the Department of Science and Technology, Government of India. A.P.M. acknowledges grants from the Academy of Finland [grants 266431 and 271832]. I.E. acknowledges the Israel Science Foundation [ISF966/17] and the Howard Hughes Medical Institute [International Research Scholar Grant 55008730]. B.A.K. was supported by a grant from National Science Foundation (NSF) [grant NSFIOS135442]. E.S. was supported by Discovery Grants of the Natural Science and Engineering Research Council of Canada [grants NSERC RGPIN-2016-04736 and NSERC RGPAS 492872-2016]. Publisher Copyright: © 2020 Company of Biologists Ltd. All rights reserved.

PY - 2020/3/30

Y1 - 2020/3/30

N2 - Aerial organs of plants, being highly prone to local injuries, require tissue restoration to ensure their survival. However, knowledge of the underlying mechanism is sparse. In this study, we mimicked natural injuries in growing leaves and stems to study the reunion between mechanically disconnected tissues. We show that PLETHORA (PLT) and AINTEGUMENTA (ANT) genes, which encode stem cell-promoting factors, are activated and contribute to vascular regeneration in response to these injuries. PLT proteins bind to and activate the CUC2 promoter. PLT proteins and CUC2 regulate the transcription of the local auxin biosynthesis gene YUC4 in a coherent feed-forward loop, and this process is necessary to drive vascular regeneration. In the absence of this PLT-mediated regeneration response, leaf ground tissue cells can neither acquire the early vascular identity marker ATHB8, nor properly polarise auxin transporters to specify new venation paths. The PLT-CUC2 module is required for vascular regeneration, but is dispensable for midvein formation in leaves. We reveal the mechanisms of vascular regeneration in plants and distinguish between the wound-repair ability of the tissue and its formation during normal development.

AB - Aerial organs of plants, being highly prone to local injuries, require tissue restoration to ensure their survival. However, knowledge of the underlying mechanism is sparse. In this study, we mimicked natural injuries in growing leaves and stems to study the reunion between mechanically disconnected tissues. We show that PLETHORA (PLT) and AINTEGUMENTA (ANT) genes, which encode stem cell-promoting factors, are activated and contribute to vascular regeneration in response to these injuries. PLT proteins bind to and activate the CUC2 promoter. PLT proteins and CUC2 regulate the transcription of the local auxin biosynthesis gene YUC4 in a coherent feed-forward loop, and this process is necessary to drive vascular regeneration. In the absence of this PLT-mediated regeneration response, leaf ground tissue cells can neither acquire the early vascular identity marker ATHB8, nor properly polarise auxin transporters to specify new venation paths. The PLT-CUC2 module is required for vascular regeneration, but is dispensable for midvein formation in leaves. We reveal the mechanisms of vascular regeneration in plants and distinguish between the wound-repair ability of the tissue and its formation during normal development.

KW - Arabidopsis

KW - Auxin

KW - CUC2

KW - PIN1

KW - PLT

KW - Vascular regeneration

KW - Wound repair

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DO - 10.1242/dev.185710

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SN - 0950-1991

VL - 147

JO - Development (Cambridge)

JF - Development (Cambridge)

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M1 - 185710

ER -

A coherent feed-forward loop drives vascular regeneration in damaged aerial organs of plants growing in a normal developmental context

Abstract

Bibliographical note

Keywords

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