Abstract

During seedling etiolation after germination in the dark, seedlings have closed cotyledons and form an apical hook to protect the meristem as they break through the soil to reach the surface. Once in contact with light, the hook opens and cotyledons are oriented upward and separate. Hook development in the dark after seedling emergence from the seed follows three distinctly timed and sequential phases: formation, maintenance, and eventual opening. We previously identified MISREGULATED IN DARK9 (MIDA9) as a phytochrome interacting factor (PIF)-repressed gene in the dark necessary for hook development during etiolated growth. MIDA9 encodes the type 2C phosphatase PP2C.D1, and pp2c-d1/mida9 mutants exhibit open hooks in the dark. Recent evidence has described that PP2C.D1 and other PP2C.D members negatively regulate SMALL AUXIN UP RNA (SAUR)-mediated cell elongation. However, the fundamental question of the timing of PP2C.D1 action (and possibly other members of the PP2C.D family) during hook development remains to be addressed. Here, we show that PP2C.D1 is required immediately after germination to form the hook. pp2c.d1/mida9 shows reduced cell expansion in the outer layer of the hook and, therefore, does not establish the differential cell growth necessary for hook formation, indicating that PP2C.D1 is necessary to promote cell elongation during this early stage. Additionally, genetic analyses of single and high order mutants in PP2C.D1, PP2C.D2, and PP2C.D5 demonstrate that the three PP2C.Ds act collectively and sequentially during etiolation: whereas PP2C.D1 dominates hook formation, PP2C.D2 is necessary during the maintenance phase, and PP2C.D5 acts to prevent opening during the third phase together with PP2C.D1 and PP2C.D2. Finally, we uncover a possible connection of PP2C.D1 levels with ethylene physiology, which could help optimize hook formation during post-germinative growth in the dark.

Highlights

  • When germination takes place in the dark, young seedlings adopt a developmental strategy called skotomorphogenesis or etiolated growth, which is energetically sustained by seed reserves

  • Much progress has been achieved in the past years, how phytochrome interacting factor (PIF) impose the different aspects of deetiolation during seedling establishment still remains incomplete

  • Our laboratory previously identified the PIF3-regulated MISREGULATED IN DARK9 (MIDA9) encoding the type-2C phosphatase PP2C.D1 as a gene involved in hook development (Sentandreu et al, 2011)

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Summary

Introduction

When germination takes place in the dark, young seedlings adopt a developmental strategy called skotomorphogenesis or etiolated growth, which is energetically sustained by seed reserves This dark-growth strategy is characterized by fast hypocotyl elongation to rapidly reach the soil surface, together with the presence of an apical hook and appressed cotyledons, which protect the apical meristem from damage while pushing through the soil (Wei et al, 1994; Gommers and Monte, 2018). Cell expansion is inhibited in the inner (concave) edge of the hook, while cell division and expansion are promoted in the outer (convex) border (Silk and Erickson, 1979; Raz and Koornneef, 2001; Vandenbussche et al, 2010), which forms an apical hook bending of the hypocotyl apex This asymmetrical cell expansion is caused by an auxin maximum in the concave part of the apical hook. It has been proposed that both GAs and ET modulate asymmetrical auxin distribution depending on the apical hook development (Vandenbussche et al, 2010; Zádníková et al, 2010)

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