A Model of Differential Growth-Guided Apical Hook Formation in Plants

Abstract

Differential cell growth enables flexible organ bending in the presence of environmental signals such as light or gravity. A prominent example of the developmental processes based on differential cell growth is the formation of the apical hook that protects the fragile shoot apical meristem when it breaks through the soil during germination. Here, we combined in silico and in vivo approaches to identify a minimal mechanism producing auxin gradient-guided differential growth during the establishment of the apical hook in the model plant Arabidopsis thaliana Computer simulation models based on experimental data demonstrate that asymmetric expression of the PIN-FORMED auxin efflux carrier at the concave (inner) versus convex (outer) side of the hook suffices to establish an auxin maximum in the epidermis at the concave side of the apical hook. Furthermore, we propose a mechanism that translates this maximum into differential growth, and thus curvature, of the apical hook. Through a combination of experimental and in silico computational approaches, we have identified the individual contributions of differential cell elongation and proliferation to defining the apical hook and reveal the role of auxin-ethylene crosstalk in balancing these two processes.

Functional Analysis of the Arabidopsis thaliana CDPK-Related Kinase Family: AtCRK1 Regulates Responses to Continuous Light

“…Hypocotyl bending in dark-germinated seedlings was also delayed in all At crk mutants ( Figure 4 D). Defects in gravitropic response suggested, that in analogy to At CRK5 , the other AtCRK genes may also be implicated in auxin transport regulation, which is essential for proper root or hypocotyl bending during gravitropic stimulation [ 15 , 30 , 31 , 32 ].…”

Role of Phytohormones and Light in De-etiolation

“…Ethylene and GA also participate in the development of the apical hook. Ethylene promotes the creation and maintenance of an auxin concentration gradient [13]. GA modifies the role of auxin and ethylene in hook development [14].…”

Seedling Establishment: A Dimmer Switch-Regulated Process between Dark and Light Signaling

“…3A). This asymmetrical cell expansion is caused by an auxin maximum in the concave part of the hook, created by auxin influx and outflux carriers (AUXIN1 [AUX1] and LIKE-AUX1, and PIN-FORMED [PIN] proteins, respectively) in the epidermal cells of the young hypocotyl (Box 2; Zádníková et al, 2010Zádníková et al, , 2016Farquharson, 2017). In darkness, PHYTOCHROME INTERACTING FACTORs (PIFs; Box 1; reviewed in this Focus Issue by Pham et al, 2018) enhance auxin synthesis and signaling, and the synthesis of two other important hormones in hook formation and maintenance, ethylene (ET) and gibberellic acid (GA; Box 2; for review, see Mazzella et al, 2014).…”

“…In darkness, PHYTOCHROME INTERACTING FACTORs (PIFs; Box 1; reviewed in this Focus Issue by Pham et al, 2018) enhance auxin synthesis and signaling, and the synthesis of two other important hormones in hook formation and maintenance, ethylene (ET) and gibberellic acid (GA; Box 2; for review, see Mazzella et al, 2014). ET signaling via transcription factors ETHYLENE INSENSITIVE3 (EIN3) and EIN3-LIKE1 (EIL1) induces local PIN gene expression in the epidermis and auxin transport ( Zádníková et al, 2016). Accordingly, exogenous treatment with ET causes exaggerated hooks in Arabidopsis (Gallego-Bartolomé et al, 2011).…”

“…During the heterotrophic phase in darkness, PIF1 and PIF3 are negative regulators of chloroplast development, particularly of tetrapyrrole biosynthesis genes (Huq et al, 2004;Stephenson et al, 2009), and transcriptionally suppress together with EIN3 (which is stabilized by soil pressure-enhanced ET production; see Box 2; Lau and Deng, 2010;Leivar and Monte, 2014;de Lucas and Prat, 2014;Chaiwanon et al, 2016;de Wit et al, 2016a;Hornitschek et al, 2012;Pfeiffer et al, 2014;Zádníková et al, 2016;Li et al, 1996;Symons et al, 2002;Oh et al, 2012;Shahnejat-Bushehri et al, 2016;Li and He, 2016;Feng et al, 2008;de Lucas et al, 2008;Guzman and Ecker, 1990;Zhong et al, 2012;Jeong et al, 2016;Shi et al, 2016;Dong et al, 2017) chloroplast development genes . Among these are the transcription factors GOLDEN2-LIKE1 (GLK1) and GLK2, which are necessary for chloroplast development (Fitter et al, 2002;Oh and Montgomery, 2014), and target genes involved in chlorophyll biosynthesis, light harvesting, and electron transport (Waters et al, 2009).…”