Crosstalk Complexities between Auxin, Cytokinin, and Ethylene in Arabidopsis Root Development: From Experiments to Systems Modeling, and Back Again

Abstract

Understanding how hormones and genes interact to coordinate plant growth in a changing environment is a major challenge in plant developmental biology. Auxin, cytokinin, and ethylene are three important hormones that regulate many aspects of plant development. This review critically evaluates the crosstalk between the three hormones in Arabidopsis root development. We integrate a variety of experimental data into a crosstalk network, which reveals multiple layers of complexity in auxin, cytokinin, and ethylene crosstalk. In particular, data integration reveals an additional, largely overlooked link between the ethylene and cytokinin pathways, which acts through a phosphorelay mechanism. This proposed link addresses outstanding questions on whether ethylene application promotes or inhibits receptor kinase activity of the ethylene receptors. Elucidating the complexity in auxin, cytokinin, and ethylene crosstalk requires a combined experimental and systems modeling approach. We evaluate important modeling efforts for establishing how crosstalk between auxin, cytokinin, and ethylene regulates patterning in root development. We discuss how a novel methodology that iteratively combines experiments with systems modeling analysis is essential for elucidating the complexity in crosstalk of auxin, cytokinin, and ethylene in root development. Finally, we discuss the future challenges from a combined experimental and modeling perspective.

1-Aminocyclopropane 1-Carboxylic Acid and Its Emerging Role as an Ethylene-Independent Growth Regulator

“…There is a complex crosstalk between ethylene and other plant hormones at the level of signaling and/or biosynthesis, the latter of which includes both transcriptional and posttranscriptional regulation of ACS (reviewed in Kazan and Manners, 2012;Muday et al, 2012;Van de Poel et al, 2015;Shigenaga and Argueso, 2016;Hu et al, 2017;Liu et al, 2017;Zemlyanskaya et al, 2018;Bürger and Chory, 2019;Qin et al, 2019). For example, cytokinin and brassinosteroid additively increase the stability of type-2 ACS proteins independently of their TOE domains ).…”

Crosstalk with Jasmonic Acid Integrates Multiple Responses in Plant Development

“…As JAZs and MYC2 are key factors in plant growth and development as positive and negative regulators, respectively, they may mediate JA-dependent growth inhibition under stress conditions [12][13][14].Plant hormones have their own specific biosynthetic and signaling pathways, but their roles in plant development and physiology overlap. This suggests that plant hormones modulate plant growth and physiology through interactions with other hormones, and the extensive interplay between auxin and cytokinin in the regulation of all aspects of plant growth and development supports this idea [15,16]. JA mediates the plant response to biotic and abiotic stresses through interaction with salicylic acid, ethylene, and abscisic acid (ABA), and details of this crosstalk and its underlying molecular mechanisms have been well reported in previous studies [3,[17][18][19].…”

Canonical and noncanonical ethylene signaling pathways that regulate Arabidopsis susceptibility to the cyst nematode Heterodera schachtii

“…4a,c). Previous protein-protein interaction analyses revealed that ETR1 interacts with key components of the cytokinin signaling pathway, including the Arabidopsis histidine-containing phosphotransfer proteins (AHPs) and response regulators (ARRs) (Urao et al, 2000;Dortay et al, 2008;Scharein et al, 2008;Liu et al, 2017). ETR1 has a functional his kinase (Gamble et al, 1998;Moussatche & Klee, 2004).…”

“…To further test this possibility, we quantified the expression of two type-A ARRs (ARR5 and ARR7), in etr1-6 and Col-0 plants under both infected and noninfected conditions. These ARRs were selected because they have been shown previously to change expression in the syncytium formed by H. schachtii in Arabidopsis (Szakasits et al, 2009;Siddique et al, 2015), in addition to their potential role in mediating the crosstalk between ethylene and cytokinin signaling (Liu et al, 2017). Under noninfected conditions, the expression of ARR5 and ARR7 was downregulated in etr1-6 compared to Col-0 plants (Fig.…”