TY - JOUR

T1 - Salicylic Acid Affects Root Meristem Patterning via Auxin Distribution in a Concentration-Dependent Manner

AU - Pasternak, Taras

AU - Groot, Edwin P.

AU - Kazantsev, Fedor V.

AU - Teale, William

AU - Omelyanchuk, Nadya

AU - Kovrizhnykh, Vasilina

AU - Palme, Klaus

AU - Mironova, Victoria V.

N1 - Funding Information: 1This work was supported by Bundesministerium für Forschung und Technologie (German Ministry for Research and Technology) (BMBF SYSTEC; BMBF FKZ031B0503B and 031B0556); Deutsche Forschungsgemeinschaft (DFG), the Excellence Initiative of the German Federal and State Governments (EXC 294); Deutsche Forschungsgemeinschaft (DFG) German Research Foundation (SFB746, INST 39/839,840,841); and Deutsches Zentrum für Luft-und Raumfahrt (German Centre for Air and Space Travel) (DLR 50WB1022). Russian participants were supported by the Russian Science Foundation. Image analysis, statistical analysis, and overall management of the project were supported by RSF 18-74-10008. Mathematical modelling was supported by RSF 17-74-10102. Support was also provided by the Shandong “Foreign experts double hundred” Program (WST2017008, to E.G.) 2These authors contributed equally to this article. 3Senior author. 4Author for contact: victoria.v.mironova@gmail.com The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (www.plantphysiol.org) is: Victoria V. Mironova (victoria.v.mironova@gmail.com). Funding Information: This work was supported by Bundesministerium f?r Forschung und Technologie (German Ministry for Research and Technology) (BMBF SYSTEC; BMBF FKZ031B0503B and 031B0556); Deutsche Forschungsgemeinschaft (DFG), the Excellence Initiative of the German Federal and State Governments (EXC 294); Deutsche Forschungsgemeinschaft (DFG) German Research Foundation (SFB746, INST 39/839,840,841); and Deutsches Zentrum f?r Luftund Raumfahrt (German Centre for Air and Space Travel) (DLR 50WB1022). Russian participants were supported by the Russian Science Foundation. Image analysis, statistical analysis, and overall management of the project were supported by RSF 18-74-10008. Mathematical modelling was supported by RSF 17-74-10102. Support was also provided by the Shandong ?Foreign experts double hundred? Program (WST2017008, to E.G.) This work could not have been accomplished without the help of Thorsten Schmidt, Thomas Haser, and Franck Ditengou who provided support, suggestions, and materials. We also gratefully acknowledge excellent technical support from Roland Nitschke, Elena Ubogoeva, and Daria Novikova, Viktoriya Lavrekha. The numerical simulations were performed on the Core center facility ?Bioinformatics? of the Siberian Supercomputer Center RAS. V.V.M. gratefully acknowledges Dmitri Zimin and his Dynasty Foundation for support in the beginning of the project without which the work would not have been done. Publisher Copyright: © 2019 American Society of Plant Biologists.

PY - 2019/7/1

Y1 - 2019/7/1

N2 - The phytohormone salicylic acid (SA) is well known for its induction of pathogenesis-related proteins and systemic acquired resistance; SA also has specific effects on plant growth and development. Here we analyzed the effect of SA on Arabidopsis (Arabidopsis thaliana) root development. We show that exogenous SA treatment at low (below 50 µM) and high (greater than 50 µM) concentrations affect root meristem development in two different PR1-independent ways. Low-concentration SA promoted adventitious roots and altered architecture of the root apical meristem, whereas high-concentration SA inhibited all growth processes in the root. All exposures to exogenous SA led to changes in auxin synthesis and transport. A wide range of SA treatment concentrations activated auxin synthesis, but the effect of SA on auxin transport was dose dependent. Mathematical modeling of auxin synthesis and transport predicted auxin accumulation or depletion in the root tip following low- or high-concentration SA treatments, respectively. SA-induced auxin accumulation led to the formation of more layers of columella initials, an additional cortical cell layer (middle cortex), and extra files of epidermis, cortex, and endodermis cells. Suppression of SHORT ROOT and activation of CYCLIN D6;1 mediated the changes in radial architecture of the root. We propose that low-concentration SA plays an important role in shaping root meristem structure and root system architecture.

AB - The phytohormone salicylic acid (SA) is well known for its induction of pathogenesis-related proteins and systemic acquired resistance; SA also has specific effects on plant growth and development. Here we analyzed the effect of SA on Arabidopsis (Arabidopsis thaliana) root development. We show that exogenous SA treatment at low (below 50 µM) and high (greater than 50 µM) concentrations affect root meristem development in two different PR1-independent ways. Low-concentration SA promoted adventitious roots and altered architecture of the root apical meristem, whereas high-concentration SA inhibited all growth processes in the root. All exposures to exogenous SA led to changes in auxin synthesis and transport. A wide range of SA treatment concentrations activated auxin synthesis, but the effect of SA on auxin transport was dose dependent. Mathematical modeling of auxin synthesis and transport predicted auxin accumulation or depletion in the root tip following low- or high-concentration SA treatments, respectively. SA-induced auxin accumulation led to the formation of more layers of columella initials, an additional cortical cell layer (middle cortex), and extra files of epidermis, cortex, and endodermis cells. Suppression of SHORT ROOT and activation of CYCLIN D6;1 mediated the changes in radial architecture of the root. We propose that low-concentration SA plays an important role in shaping root meristem structure and root system architecture.

KW - SYSTEMIC ACQUIRED-RESISTANCE

KW - PROGRAMMED CELL-DEATH

KW - TRANSCRIPTION FACTOR

KW - GENE-EXPRESSION

KW - APICAL MERISTEM

KW - GROUND TISSUE

KW - GROWTH

KW - PROTEIN

KW - BIOSYNTHESIS

KW - ORGANIZATION

UR - http://www.scopus.com/inward/record.url?scp=85069234325&partnerID=8YFLogxK

U2 - 10.1104/pp.19.00130

DO - 10.1104/pp.19.00130

M3 - Article

C2 - 31036755

AN - SCOPUS:85069234325

VL - 180

SP - 1725

EP - 1739

JO - Plant Physiology

JF - Plant Physiology

SN - 0032-0889

IS - 3

ER -