Root gravitropism is regulated by a transient lateral auxin gradient controlled by a tipping-point mechanism

Leah R. Band, Darren M. Wells, Antoine Larrieu, Jianyong Sun, Alistair M. Middleton, Andrew P. French, Géraldine Brunoud, Ethel Mendocilla Sato, Michael H. Wilson, Benjamin Péret, Marina Oliva, Ranjan Swarup, Ilkka Sairanen, Geraint Parry, Karin Ljung, Tom Beeckman, Jonathan M. Garibaldi, Mark Estelle, Markus R. Owen, Kris Vissenberg & 5 others T. Charlie Hodgman, Tony P. Pridmore, John R. King, Teva Vernoux, Malcolm J. Bennett

Research output: Contribution to journalArticle

164 Citations (Scopus)

Abstract

Gravity profoundly influences plant growth and development. Plants respond to changes in orientation by using gravitropic responses to modify their growth. Cholodny and Went hypothesized over 80 years ago that plants bend in response to a gravity stimulus by generating a lateral gradient of a growth regulator at an organ's apex, later found to be auxin. Auxin regulates root growth by targeting Aux/IAA repressor proteins for degradation. We used an Aux/IAA-based reporter, domain II (DII)-VENUS, in conjunction with a mathematical model to quantify auxin redistribution following a gravity stimulus. Our multidisciplinary approach revealed that auxin is rapidly redistributed to the lower side of the root within minutes of a 90° gravity stimulus. Unexpectedly, auxin asymmetry was rapidly lost as bending root tips reached an angle of 40° to the horizontal. We hypothesize roots use a “tipping point” mechanism that operates to reverse the asymmetric auxin flow at the midpoint of root bending. These mechanistic insights illustrate the scientific value of developing quantitative reporters such as DII-VENUS in conjunction with parameterized mathematical models to provide high-resolution kinetics of hormone redistribution.
Original languageEnglish
Pages (from-to)4668–4673
Number of pages6
JournalProceedings of the National Academy of Sciences
Volume109
Issue number12
DOIs
Publication statusPublished - Mar 2012
Externally publishedYes

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gravitropism
auxins
gravity
indole acetic acid
mathematical models
protein degradation
growth regulators
root tips
plant development
root growth
growth and development
hormones
plant growth
kinetics

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Band, L. R., Wells, D. M., Larrieu, A., Sun, J., Middleton, A. M., French, A. P., ... Bennett, M. J. (2012). Root gravitropism is regulated by a transient lateral auxin gradient controlled by a tipping-point mechanism. Proceedings of the National Academy of Sciences, 109(12), 4668–4673. https://doi.org/10.1073/pnas.1201498109
Band, Leah R. ; Wells, Darren M. ; Larrieu, Antoine ; Sun, Jianyong ; Middleton, Alistair M. ; French, Andrew P. ; Brunoud, Géraldine ; Sato, Ethel Mendocilla ; Wilson, Michael H. ; Péret, Benjamin ; Oliva, Marina ; Swarup, Ranjan ; Sairanen, Ilkka ; Parry, Geraint ; Ljung, Karin ; Beeckman, Tom ; Garibaldi, Jonathan M. ; Estelle, Mark ; Owen, Markus R. ; Vissenberg, Kris ; Hodgman, T. Charlie ; Pridmore, Tony P. ; King, John R. ; Vernoux, Teva ; Bennett, Malcolm J. / Root gravitropism is regulated by a transient lateral auxin gradient controlled by a tipping-point mechanism. In: Proceedings of the National Academy of Sciences. 2012 ; Vol. 109, No. 12. pp. 4668–4673.
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abstract = "Gravity profoundly influences plant growth and development. Plants respond to changes in orientation by using gravitropic responses to modify their growth. Cholodny and Went hypothesized over 80 years ago that plants bend in response to a gravity stimulus by generating a lateral gradient of a growth regulator at an organ's apex, later found to be auxin. Auxin regulates root growth by targeting Aux/IAA repressor proteins for degradation. We used an Aux/IAA-based reporter, domain II (DII)-VENUS, in conjunction with a mathematical model to quantify auxin redistribution following a gravity stimulus. Our multidisciplinary approach revealed that auxin is rapidly redistributed to the lower side of the root within minutes of a 90° gravity stimulus. Unexpectedly, auxin asymmetry was rapidly lost as bending root tips reached an angle of 40° to the horizontal. We hypothesize roots use a “tipping point” mechanism that operates to reverse the asymmetric auxin flow at the midpoint of root bending. These mechanistic insights illustrate the scientific value of developing quantitative reporters such as DII-VENUS in conjunction with parameterized mathematical models to provide high-resolution kinetics of hormone redistribution.",
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Band, LR, Wells, DM, Larrieu, A, Sun, J, Middleton, AM, French, AP, Brunoud, G, Sato, EM, Wilson, MH, Péret, B, Oliva, M, Swarup, R, Sairanen, I, Parry, G, Ljung, K, Beeckman, T, Garibaldi, JM, Estelle, M, Owen, MR, Vissenberg, K, Hodgman, TC, Pridmore, TP, King, JR, Vernoux, T & Bennett, MJ 2012, 'Root gravitropism is regulated by a transient lateral auxin gradient controlled by a tipping-point mechanism', Proceedings of the National Academy of Sciences, vol. 109, no. 12, pp. 4668–4673. https://doi.org/10.1073/pnas.1201498109

Root gravitropism is regulated by a transient lateral auxin gradient controlled by a tipping-point mechanism. / Band, Leah R.; Wells, Darren M.; Larrieu, Antoine; Sun, Jianyong; Middleton, Alistair M.; French, Andrew P.; Brunoud, Géraldine; Sato, Ethel Mendocilla; Wilson, Michael H.; Péret, Benjamin; Oliva, Marina; Swarup, Ranjan; Sairanen, Ilkka; Parry, Geraint; Ljung, Karin; Beeckman, Tom; Garibaldi, Jonathan M.; Estelle, Mark; Owen, Markus R.; Vissenberg, Kris; Hodgman, T. Charlie; Pridmore, Tony P.; King, John R.; Vernoux, Teva; Bennett, Malcolm J.

In: Proceedings of the National Academy of Sciences, Vol. 109, No. 12, 03.2012, p. 4668–4673.

Research output: Contribution to journalArticle

TY - JOUR

T1 - Root gravitropism is regulated by a transient lateral auxin gradient controlled by a tipping-point mechanism

AU - Band, Leah R.

AU - Wells, Darren M.

AU - Larrieu, Antoine

AU - Sun, Jianyong

AU - Middleton, Alistair M.

AU - French, Andrew P.

AU - Brunoud, Géraldine

AU - Sato, Ethel Mendocilla

AU - Wilson, Michael H.

AU - Péret, Benjamin

AU - Oliva, Marina

AU - Swarup, Ranjan

AU - Sairanen, Ilkka

AU - Parry, Geraint

AU - Ljung, Karin

AU - Beeckman, Tom

AU - Garibaldi, Jonathan M.

AU - Estelle, Mark

AU - Owen, Markus R.

AU - Vissenberg, Kris

AU - Hodgman, T. Charlie

AU - Pridmore, Tony P.

AU - King, John R.

AU - Vernoux, Teva

AU - Bennett, Malcolm J.

PY - 2012/3

Y1 - 2012/3

N2 - Gravity profoundly influences plant growth and development. Plants respond to changes in orientation by using gravitropic responses to modify their growth. Cholodny and Went hypothesized over 80 years ago that plants bend in response to a gravity stimulus by generating a lateral gradient of a growth regulator at an organ's apex, later found to be auxin. Auxin regulates root growth by targeting Aux/IAA repressor proteins for degradation. We used an Aux/IAA-based reporter, domain II (DII)-VENUS, in conjunction with a mathematical model to quantify auxin redistribution following a gravity stimulus. Our multidisciplinary approach revealed that auxin is rapidly redistributed to the lower side of the root within minutes of a 90° gravity stimulus. Unexpectedly, auxin asymmetry was rapidly lost as bending root tips reached an angle of 40° to the horizontal. We hypothesize roots use a “tipping point” mechanism that operates to reverse the asymmetric auxin flow at the midpoint of root bending. These mechanistic insights illustrate the scientific value of developing quantitative reporters such as DII-VENUS in conjunction with parameterized mathematical models to provide high-resolution kinetics of hormone redistribution.

AB - Gravity profoundly influences plant growth and development. Plants respond to changes in orientation by using gravitropic responses to modify their growth. Cholodny and Went hypothesized over 80 years ago that plants bend in response to a gravity stimulus by generating a lateral gradient of a growth regulator at an organ's apex, later found to be auxin. Auxin regulates root growth by targeting Aux/IAA repressor proteins for degradation. We used an Aux/IAA-based reporter, domain II (DII)-VENUS, in conjunction with a mathematical model to quantify auxin redistribution following a gravity stimulus. Our multidisciplinary approach revealed that auxin is rapidly redistributed to the lower side of the root within minutes of a 90° gravity stimulus. Unexpectedly, auxin asymmetry was rapidly lost as bending root tips reached an angle of 40° to the horizontal. We hypothesize roots use a “tipping point” mechanism that operates to reverse the asymmetric auxin flow at the midpoint of root bending. These mechanistic insights illustrate the scientific value of developing quantitative reporters such as DII-VENUS in conjunction with parameterized mathematical models to provide high-resolution kinetics of hormone redistribution.

U2 - 10.1073/pnas.1201498109

DO - 10.1073/pnas.1201498109

M3 - Article

VL - 109

SP - 4668

EP - 4673

JO - Proceedings of the National Academy of Sciences of the United States of America

JF - Proceedings of the National Academy of Sciences of the United States of America

SN - 0027-8424

IS - 12

ER -