Growth asymmetry precedes differential auxin response during apical hook initiation in Arabidopsis

Abstract

The development of a hook‐like structure at the apical part of the soil‐emerging organs has fascinated botanists for centuries, but how it is initiated remains unclear. Here, we demonstrate with high‐throughput infrared imaging and 2‐D clinostat treatment that, when gravity‐induced root bending is absent, apical hook formation still takes place. In such scenarios, hook formation begins with a de novo growth asymmetry at the apical part of a straightly elongating hypocotyl. Remarkably, such de novo asymmetric growth, but not the following hook enlargement, precedes the establishment of a detectable auxin response asymmetry, and is largely independent of auxin biosynthesis, transport and signaling. Moreover, we found that functional cortical microtubule array is essential for the following enlargement of hook curvature. When microtubule array was disrupted by oryzalin, the polar localization of PIN proteins and the formation of an auxin maximum became impaired at the to‐be‐hook region. Taken together, we propose a more comprehensive model for apical hook initiation, in which the microtubule‐dependent polar localization of PINs may mediate the instruction of growth asymmetry that is either stochastically taking place, induced by gravitropic response, or both, to generate a significant auxin gradient that drives the full development of the apical hook.

Modulation of Receptor-like Trans-Membrane Kinase 1 nuclear localisation by DA1 peptidases in Arabidopsis

“…Apical hooks are formed by asymmetric cell elongation established by a gradient of auxin distribution, from higher levels at the concave surface to lower levels at the convex surface that drives differential cell growth (30). Nuclear-localised TMK1 is present at higher levels on the concave side of the apical hook, suggesting higher auxin levels on the concave side increase the cleavage and nuclear localization of TMK1 (25).…”

Auxin signaling: Research advances over the past 30 years

“…Recent studies on the formation and maintenance of the apical hook (Figure 3A, B), which protects the cotyledons and shoot apical meristem from mechanical damage during seedling emergence from the soil, revealed another auxin signaling mechanism. The auxin level at the convex side of the apical hook is relatively low, promoting cell elongation, whereas the auxin level at the concave side is high (Peng et al, 2021), inhibiting this process (McLaughlin et al, 2021). The wei8-3 tar2-1 mutant, which is deficient in auxin biosynthesis, fails to produce high auxin levels at the concave side of the apical hook, resulting in ineffective inhibition of cell elongation at the concave side (Cao et al, 2019).…”

New Wine in an Old Bottle: Utilizing Chemical Genetics to Dissect Apical Hook Development

“…Besides transport, uxin perception is also a key regulating point for apical hook development. Several chemical regulators that target the auxin receptor have been reported, such as auxinole as an antagonist [ 69 ], fluorescent auxin analogs [ 70 ], and selective agonists for specific subsets of AUX/IAA [ 71 ], among which auxinole was applied to dissect the developmental processes of the apical hook [ 15 ]. In addition, an orthogonal auxin–TIR1 receptor pair (convex IAA–concave TIR1) has been developed [ 72 ], providing a strategy for the precise manipulation of auxin signal.…”

“…Upstream of the polar auxin transport events, functional microtubule arrays are indispensable for the correct distribution of auxin transporters, and guarantee the establishment of auxin asymmetry [ 73 , 74 ]. The application of 50 mM oryzalin completely abolished the normal apical hook formation in Col-0, and a lower concentration (200 nM) could revert the positive contribution of the external mechanical constraint on apical hook development in the ktn1-5 mutant [ 15 , 73 ], hinting at a fundamental role of functional microtubule arrays in hook development. Moreover, a previous chemical screening using the co-treatment of compounds with ACC, a precursor of ethylene, identified several interesting compounds that either promote or inhibit the apical hook [ 75 ].…”

“…A high concentration of auxin accumulates at the concave side of the apical hook, which activates AUXIN RESPONSE FACTORs (ARFs) to promote the transcription of D CLADE TYPE 2C PROTEIN PHOSPHATASE ( PP2C-D1 ), a negative regulator of cell elongation, to establish growth asymmetry [ 14 ]. Peng et al demonstrated that HLS1 is necessary for the establishment of polar auxin transport (PAT) after apical hook initiation; however, the relationship between HLS1 and PAT is still unclear [ 15 ]. To date, possibly due to genetic redundancy or lethal mutation, only one regulator downstream of HLS1 has been identified.…”