TY - JOUR

T1 - Cytokinins regulate spatially specific ethylene production to control root growth in Arabidopsis

AU - Yamoune, Amel

AU - Zdarska, Marketa

AU - Depaepe, Thomas

AU - Rudolfova, Anna

AU - Skalak, Jan

AU - Berendzen, Kenneth Wayne

AU - Mira-Rodado, Virtudes

AU - Fitz, Michael

AU - Pekarova, Blanka

AU - Nicolas Mala, Katrina Leslie

AU - Tarr, Paul

AU - Spackova, Eliska

AU - Tomovicova, Lucia

AU - Parizkova, Barbora

AU - Franczyk, Abigail

AU - Kovacova, Ingrid

AU - Dolgikh, Vladislav

AU - Zemlyanskaya, Elena

AU - Pernisova, Marketa

AU - Novak, Ondrej

AU - Meyerowitz, Elliot

AU - Harter, Klaus

AU - Van Der Straeten, Dominique

AU - Hejatko, Jan

N1 - This work was supported by the Ministry of Education, Youth and Sports of the Czech Republic under the projects TANGENC ( CZ.02.01.01/00/22_008/0004581 ) and LUAUS24277. The work was supported by the German Research Foundation (CRC 1101 project D02) and the Howard Hughes Medical Institute (to E.M.M.). The work of E.Z. and V.D. was supported by the Russian Science Foundation (20-14-00140).

PY - 2024/11/11

Y1 - 2024/11/11

N2 - Two principal growth regulators, cytokinins and ethylene, are known to interact in the regulation of plant growth. However, information about the underlying molecular mechanism and positional specificity of cytokinin/ethylene crosstalk in the control of root growth is scarce. We have identified the spatial specificity of cytokinin-regulated root elongation and root apical meristem (RAM) size, both of which we demonstrate to be dependent on ethylene biosynthesis. Upregulation of the cytokinin biosynthetic gene ISOPENTENYLTRANSFERASE (IPT) in proximal and peripheral tissues leads to both root and RAM shortening. By contrast, IPT activation in distal and inner tissues reduces RAM size while leaving the root length comparable to that of mock-treated controls. We show that cytokinins regulate two steps specific to ethylene biosynthesis: production of the ethylene precursor 1-aminocyclopropane-1-carboxylate (ACC) by ACC SYNTHASEs (ACSs) and its conversion to ethylene by ACC OXIDASEs (ACOs). We describe cytokinin- and ethylene-specific regulation controlling the activity of ACSs and ACOs that are spatially discrete along both proximo/distal and radial root axes. Using direct ethylene measurements, we identify ACO2, ACO3, and ACO4 as being responsible for ethylene biosynthesis and ethylene-regulated root and RAM shortening in cytokinin-treated Arabidopsis. Direct interaction between ARABIDOPSIS RESPONSE REGULATOR 2 (ARR2), a member of the multistep phosphorelay cascade, and the C-terminal portion of ETHYLENE INSENSITIVE 2 (EIN2-C), a key regulator of canonical ethylene signaling, is involved in the cytokinin-induced, ethylene-mediated control of ACO4. We propose tight cooperation between cytokinin and ethylene signaling in the spatially specific regulation of ethylene biosynthesis as a key aspect of the hormonal control of root growth.

AB - Two principal growth regulators, cytokinins and ethylene, are known to interact in the regulation of plant growth. However, information about the underlying molecular mechanism and positional specificity of cytokinin/ethylene crosstalk in the control of root growth is scarce. We have identified the spatial specificity of cytokinin-regulated root elongation and root apical meristem (RAM) size, both of which we demonstrate to be dependent on ethylene biosynthesis. Upregulation of the cytokinin biosynthetic gene ISOPENTENYLTRANSFERASE (IPT) in proximal and peripheral tissues leads to both root and RAM shortening. By contrast, IPT activation in distal and inner tissues reduces RAM size while leaving the root length comparable to that of mock-treated controls. We show that cytokinins regulate two steps specific to ethylene biosynthesis: production of the ethylene precursor 1-aminocyclopropane-1-carboxylate (ACC) by ACC SYNTHASEs (ACSs) and its conversion to ethylene by ACC OXIDASEs (ACOs). We describe cytokinin- and ethylene-specific regulation controlling the activity of ACSs and ACOs that are spatially discrete along both proximo/distal and radial root axes. Using direct ethylene measurements, we identify ACO2, ACO3, and ACO4 as being responsible for ethylene biosynthesis and ethylene-regulated root and RAM shortening in cytokinin-treated Arabidopsis. Direct interaction between ARABIDOPSIS RESPONSE REGULATOR 2 (ARR2), a member of the multistep phosphorelay cascade, and the C-terminal portion of ETHYLENE INSENSITIVE 2 (EIN2-C), a key regulator of canonical ethylene signaling, is involved in the cytokinin-induced, ethylene-mediated control of ACO4. We propose tight cooperation between cytokinin and ethylene signaling in the spatially specific regulation of ethylene biosynthesis as a key aspect of the hormonal control of root growth.

KW - ACC OXIDASE

KW - ACC SYNTHASE

KW - Arabidopsis

KW - cytokinin

KW - ethylene

KW - multistep phosphorelay

KW - Ethylenes/metabolism

KW - Arabidopsis/genetics

KW - Cytokinins/metabolism

KW - Plant Roots/growth & development

KW - Gene Expression Regulation, Plant

KW - Arabidopsis Proteins/genetics

UR - https://www.scopus.com/record/display.uri?eid=2-s2.0-85200240330&origin=inward&txGid=4e7dd8af0da09188aeaeadb39feac60e

UR - https://www.mendeley.com/catalogue/36ab450c-4054-3f39-b928-502cb6d87c1e/

U2 - 10.1016/j.xplc.2024.101013

DO - 10.1016/j.xplc.2024.101013

M3 - Article

C2 - 38961625

VL - 5

JO - Plant Communications

JF - Plant Communications

SN - 2590-3462

IS - 11

M1 - 101013

ER -