The classical “Cholodny-Went theory” predicted that directional stimuli trigger the redistribution of auxin, which governs the differential growth of plant organs through potent effects on cell expansion, thereby establishing an “auxin-then-growth” paradigm; this theory has been validated for both gravitropism and phototropism in plants (reviewed in Muthert et al., 2020). During apical hook development, auxin indeed plays a crucial role: local auxin maxima define the concave side of the hook curvature (Darwin and Darwin, 1881; Beziat and Kleine-Vehn, 2018; Wang and Guo, 2019; Zhu et al., 2019). While a vast body of research has implicated auxin and diverse signaling pathways in dynamic apical hook development, few studies have focused on the earliest “initiation stage” (Zhu et al., 2019; Du et al., 2021). Recent work proposed that extended gravitropic bending from the radicle to the hypocotyl triggers the asymmetric auxin accumulation in the hook region, linking the processes of root and hypocotyl gravitropism to apical hook formation (Zhu et al., 2019). However, how asymmetric auxin distribution is initially triggered during apical hook development remains elusive. In this issue, Peng et al. (2021) used a high-throughput infrared imaging platform to observe the dynamic morphogenesis of apical hook initiation in Arabidopsis. They uncovered a temporal sequence between hypocotyl growth asymmetry and differential auxin responses during the initial stages of apical hook formation.
Peng et al. (2021) subjected young seedlings to constant rotation in a 2-D clinostat, which effectively nullifies gravity perception in the roots and hypocotyl. Under these gravity-disrupted conditions, they observed that a normal, closed apical hook still forms. In such scenarios, de novo bending takes place in an originally straightly elongating hypocotyl where auxin is evenly distributed, indicating that a root gravitropism-independent mechanism also contributes to apical hook formation. These findings provided an opportunity to further explore how a differential auxin response is first established in apical hook initiation.
Using a combinatorial imaging method, Peng et al. (2021) observed that the de novo growth asymmetry (small angle bending) at the apical part of the hypocotyl precedes the establishment of a differential auxin response (Figure 1). Genetic and pharmacological studies also demonstrated that the initiation of growth asymmetry is largely independent of auxin biosynthesis, transport and signaling. These observations prompted the authors to explore how the de novo growth asymmetry leads to larger hook curvature, and how the differential auxin response is established during these processes, as it is crucial for the subsequent stages of apical hook development.
The “bending-triggered curvature” model
Root gravity responses and stochastic growth asymmetry may trigger de novo growth asymmetry at the apical part of the hypocotyl, which could result in asymmetric mechanical constraints. The asymmetric mechanical constraints could enhance the extent of growth asymmetry directly, or may do so indirectly by regulating the microtubule-influenced polar auxin transport that sustains the formation of auxin maxima. Four representative images highlight the successive developmental stages of apical hook formation, from straight to completely curved. Green fluorescent protein (GFP) signal intensities of the auxin response reporter DR5::GFP are drawn according to figure 3 in Peng et al. (2021). Note that the auxin response remains symmetric across the curvature of the asymmetric growth stage, which is designated as the “de novo growth asymmetry”.
Notably, Peng et al. (2021) reported when young seedlings are grown in horizontal Petri dishes, the hook structure does not form if hypocotyls are in the air (no contact with the medium). These data suggest that the de novo growth asymmetry during apical hook formation could be promoted by external mechanical cues. Microtubules mediate plant mechanoresponses and tissue geometry-directed auxin distribution in other processes (Nakayama et al., 2012; Hamant et al., 2019). Indeed, the authors determined that the microtubule array-regulated polar localization of the auxin transporters PIN1 and PIN3 may mediate de novo growth asymmetry to generate a significant auxin gradient that drives full development of the apical hook.
In summary, Peng et al. (2021) showed that growth asymmetry precedes the differential auxin response during apical hook initiation. The authors propose a “growth-then-auxin” model, in which auxin response is a crucial amplifying module for a small bending-triggered large curvature, rather than the initial cue. This work thus provides intriguing insights into the mechanisms of early apical hook development.