Cytokinins regulate spatially-specific ethylene production to control root growth inArabidopsis

Abstract

The two principal growth regulators cytokinins and ethylene are known to interact in the regulation of plant growth. However, information about underlying molecular mechanism and positional specificity of the cytokinin/ethylene crosstalk in root growth control is scarce. We have identified spatial specificity of cytokinin-regulated root elongation and root apical meristem (RAM) size, both of which we demonstrate to be ethylene biosynthesis-dependent. Upregulation of the cytokinin biosynthetic gene ISOPENTENYLTRANSFERASE (IPT) in proximal and peripheral tissues leads to both root and RAM shortening. In contrast, IPT activation in distal and inner tissues reduces RAM size while leaving the root length comparable to mock-treated controls. We show that cytokinins regulate two steps specific to ethylene biosynthesis, the production of 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 the ethylene-regulated root and RAM shortening in cytokinin-treated Arabidopsis. Finally, we describe the tight cooperation between cytokinin and ethylene signaling in cytokinin-induced, ethylene-regulated control of ACO4 due to the 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.

1-Aminocyclopropane-1-carboxylic acid oxidase determines the fate of ethylene biosynthesis in a tissue-specific way to fine-tune development and stress resilience

“…In fact, it is well established that ethylene crosstalks with auxins to regulate primary root development (Stepanova et al, 2007; Swarup et al, 2007; Ruzicka et al, 2007), although the role of ACOs in this remains unstudied. Furthermore, cytokinins activate tissue-specific expression of ACO2 , ACO3 and ACO4 in Arabidopsis roots leading to an inhibition of primary root growth (Yamoune et al ., 2023). Brassinosteroids activate ACO1 expression in the root tip via BES1, and contribute to the regulation of a gravitropic response (Park et al ., 2020).…”