Molecular mechanisms and hormonal regulation underpinning morphological dormancy: a case study using Apium graveolens (Apiaceae).

Matthew Walker,Iva Pavlović,Gerhard Leubner‐Metzger,Miroslav Strnad,Danuše Tarkowská,Ondřej Novák,Kazumi Nakabayashi,Federica Marone,Tina Steinbrecher,Marta Pérez,Frances Gawthrop

doi:10.1111/tpj.15489

Abstract

Underdeveloped (small) embryos embedded in abundant endosperm tissue, and thus having morphological dormancy (MD) or morphophysiological dormancy (MPD), are considered to be the ancestral state in seed dormancy evolution. This trait is retained in the Apiaceae family, which provides excellent model systems for investigating the underpinning mechanisms. We investigated Apium graveolens (celery) MD by combined innovative imaging and embryo growth assays with the quantification of hormone metabolism, as well as the analysis of hormone and cell-wall related gene expression. The integrated experimental results demonstrated that embryo growth occurred inside imbibed celery fruits in association with endosperm degradation, and that a critical embryo size was required for radicle emergence. The regulation of these processes depends on gene expression leading to gibberellin and indole-3-acetic acid (IAA) production by the embryo and on crosstalk between the fruit compartments. ABA degradation associated with distinct spatiotemporal patterns in ABA sensitivity control embryo growth, endosperm breakdown and radicle emergence. This complex interaction between gibberellins, IAA and ABA metabolism, and changes in the tissue-specific sensitivities to these hormones is distinct from non-MD seeds. We conclude that the embryo growth to reach the critical size and the associated endosperm breakdown inside MD fruits constitute a unique germination programme.

Highlights

A diversity of seed dormancy mechanisms evolved to time germination and subsequent seedling growth in variable environments (Baskin and Baskin, 2014; Finch-Savage and Footitt, 2017)
In the fruits of most of the Apiaceae food and spice plants, the small embryo is linear and well developed into embryonic root and shoot (Figure 1a). Both morphological dormancy (MD) and morphophysiological dormancy (MPD) require that the small embryo first grows inside the seed before it can complete germination by radicle emergence (Baskin and Baskin, 2014; Zhang et al, 2019)
We found that the 13-hydroxylated biosynthetic pathway leading to GA1 as bioactive GA was dominant in celery fruits and large amounts of GA8 and GA29 accumulated in dry fruits (Figure 5c), the GA1 contents declined upon imbibition and increased only late in the phase (Figure 5a)

Summary

Introduction

A diversity of seed dormancy mechanisms evolved to time germination and subsequent seedling growth in variable environments (Baskin and Baskin, 2014; Finch-Savage and Footitt, 2017). Seed ecologists distinguish several major seed dormancy classes including nondormancy (ND), physiological dormancy (PD), morphological dormancy (MD) and morphophysiological dormancy (MPD) (Baskin and Baskin, 2014; Willis et al, 2014). These are associated with functional traits underlying the variation in germination phenology in adaptation to seasons, climates and habitats (Fernandez-Pascual et al, 2019; Finch-Savage and Footitt, 2017). An abundance of published work has revealed the underpinning molecular mechanisms of PD (e.g. Arabidopsis thaliana, Brassicaceae) and ND (e.g. Lepidium sativum, Brassicaceae) seeds in response to environmental cues

Results

Discussion

Conclusion