Cytokinin functions as an asymmetric and anti-gravitropic signal in lateral roots

Abstract

Directional organ growth allows the plant root system to strategically cover its surroundings. Intercellular auxin transport is aligned with the gravity vector in the primary root tips, facilitating downward organ bending at the lower root flank. Here we show that cytokinin signaling functions as a lateral root specific anti-gravitropic component, promoting the radial distribution of the root system. We performed a genome-wide association study and reveal that signal peptide processing of Cytokinin Oxidase 2 (CKX2) affects its enzymatic activity and, thereby, determines the degradation of cytokinins in natural Arabidopsis thaliana accessions. Cytokinin signaling interferes with growth at the upper lateral root flank and thereby prevents downward bending. Our interdisciplinary approach proposes that two phytohormonal cues at opposite organ flanks counterbalance each other’s negative impact on growth, suppressing organ growth towards gravity and allow for radial expansion of the root system.

Cytokinin dehydrogenase: a genetic target for yield improvement in wheat

“…However, cytokinin has been shown to be required for maintenance of both the shoot apical meristem and root apical meristem (Werner et al , ; Wybouw and De Rybel, ). Additionally, cytokinin is involved in regulating root system architecture in arabidopsis: it acts as a positional cue through its interaction with auxin, regulating lateral root spacing through the action of IPT and LOG4 genes (Chang et al , ), and in the gravitropic response of lateral roots (Waidmann et al , ).…”

“…Friml et al , ). Lateral roots establish a distinct gravitropic set‐point angle (GSA) (Digby and Firn, ) at an angle to gravity that differs from the primary roots and that suggests a suppressive response to gravity (Waidmann et al , ). Based on a genome‐wide association study (GWAS) of arabidopsis lines, Waidmann et al () identified a prominent peak associated with a single nucleotide polymorphism located in the AtCKX2 gene that was associated with increased GSA values, reflecting more perpendicular LR growth to gravity.…”

“…Lateral roots establish a distinct gravitropic set‐point angle (GSA) (Digby and Firn, ) at an angle to gravity that differs from the primary roots and that suggests a suppressive response to gravity (Waidmann et al , ). Based on a genome‐wide association study (GWAS) of arabidopsis lines, Waidmann et al () identified a prominent peak associated with a single nucleotide polymorphism located in the AtCKX2 gene that was associated with increased GSA values, reflecting more perpendicular LR growth to gravity. As root angle could be increased or decreased by enhancing or reducing AtCKX2 activity, respectively, Waidmann et al () concluded that cytokinin signalling defines directional lateral root growth by reducing lateral root bending after emergence, through the activity of AtCKX2 .…”

“…The plant hormone group, the cytokinins, has been strongly implicated in many aspects affecting yield, particularly grain number and size (Jameson and Song, ; Yamburenko et al , ), but including response to biotic and abiotic stressors (Cortleven et al , ; Pavlů et al , ), mineral status (Gao et al , ; Guo et al , ) and leaf senescence (Hönig et al , ; Zwack et al , ). The cytokinins, which are positive regulators of shoot growth and negative regulators of root growth (Werner et al , ), are implicated in the control of both shoot architecture (Bartrina et al , ; Han et al , ) and root system architecture (Waidmann et al , ; Werner and Schmülling, ), and crown root formation (Gao et al , ). Recent research indicates a significant negative role in the control of micronutrient uptake (Gao et al , ; Nehnevajova et al , ; Ramireddy et al , ).…”

Defying gravity: a plant’s quest for moisture

“…For example, asymmetric distribution of cytokinin has been shown to counteract auxin responses in the control lateral root branch angle, an important aspect of how roots explore their soil environment. 12 By expanding our fundamental understanding of hydrotropism, Chang et al also enhance our ability to generate different varieties of crops better suited to survival in waterlimited conditions, which will contribute to our capacity to mitigate the effects of climate change.…”