Metabolism and development – integration of micro computed tomography data and metabolite profiling reveals metabolic reprogramming from floral initiation to silique development

Anke Bellaire,Sriram Parameswaran,Isabell Weinhaeuser,Toshiro Ito,Andrea Mair,Till Ischebeck,Wolfram Weckwerth,Yannick Staedler,Jürg Schönenberger

doi:10.1111/nph.12631

Abstract

The interrelationship of morphogenesis and metabolism is a poorly studied phenomenon. The main paradigm is that development is controlled by gene expression. The aim of the present study was to correlate metabolism to early and late stages of flower and fruit development in order to provide the basis for the identification of metabolic adjustment and limitations.A highly detailed picture of morphogenesis is achieved using nondestructive micro computed tomography. This technique was used to quantify morphometric parameters of early and late flower development in an Arabidopsis thaliana mutant with synchronized flower initiation. The synchronized flower phenotype made it possible to sample enough early floral tissue otherwise not accessible for metabolomic analysis.The integration of metabolomic and morphometric data enabled the correlation of metabolic signatures with the process of flower morphogenesis. These signatures changed significantly during development, indicating a pronounced metabolic reprogramming in the tissue. Distinct sets of metabolites involved in these processes were identified and were linked to the findings of previous gene expression studies of flower development. High correlations with basic leucine zipper (bZIP) transcription factors and nitrogen metabolism genes involved in the control of metabolic carbon : nitrogen partitioning were revealed.Based on these observations a model for metabolic adjustment during flower development is proposed.

Highlights

Angiosperms are the largest group of higher plants, with 300 000–400 000 estimated species (The Angiosperm Phylogeny Group, 2009)
The aim of the present study was to correlate metabolism to early and late stages of flower and fruit development in order to provide the basis for the identification of metabolic adjustment and limitations
Flowers from a total of 14 time-points comprising developmental stages ranging from floral initiation to fruit formation were harvested for morphological analysis by photography, light microscopy (LM), scanning electron microscopy (SEM) and micro-CT

Summary

Introduction

Angiosperms are the largest group of higher plants, with 300 000–400 000 estimated species (The Angiosperm Phylogeny Group, 2009). Flower and fruit development in these plants are the most critical steps of generative reproduction. The morphology of flower development of Arabidopsis thaliana, a species of the Brassicaceae family and a model species in plant sciences, has been analysed by Smyth et al, who defined 20 stages from the appearance of the first floral meristem to the dispersal of seeds (Mu€ller, 1961; Smyth et al, 1990).

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