Metabolome and Lipidome Profiles of Populus × canescens Twig Tissues During Annual Growth Show Phospholipid-Linked Storage and Mobilization of C, N, and S.

Mutsumi Watanabe,Yariv Brotman,Florian Netzer,Heinz Rennenberg,Alisdair R Fernie,Isabel Orf,David Dubbert,Takayuki Tohge,Cornelia Herschbach,Rainer Hoefgen

doi:10.3389/fpls.2018.01292

Abstract

The temperate climax tree species Fagus sylvatica and the floodplain tree species Populus × canescens possess contrasting phosphorus (P) nutrition strategies. While F. sylvatica has been documented to display P storage and mobilization (Netzer et al., 2017), this was not observed for Populus × canescens (Netzer et al., 2018b). Nevertheless, changes in the abundance of organic bound P in gray poplar trees indicated adaptation of the P nutrition to different needs during annual growth. The present study aimed at characterizing seasonal changes in metabolite and lipid abundances in gray poplar and uncovering differences in metabolite requirement due to specific needs depending on the season. Seasonal variations in the abundance of (i) sugar-Ps and phospholipids, (ii) amino acids, (iii) sulfur compounds, and (iv) carbon metabolites were expected. It was hypothesized that seasonal changes in metabolite levels relate to N, S, and C storage and mobilization. Changes in organic metabolites binding Pi (Porg) are supposed to support these processes. Variation in triacylglycerols, in sugar-phosphates, in metabolites of the TCA cycle and in the amino acid abundance of poplar twig buds, leaves, bark, and wood were found to be linked to changes in metabolite abundances as well as to C, N, and S storage and mobilization processes. The observed changes support the view of a lack of any P storage in poplar. Yet, during dormancy, contents of phospholipids in twig bark and wood were highest probably due to frost-hardening and to its function in extra-plastidic membranes such as amyloplasts, oleosomes, and protein bodies. Consistent with this assumption, in spring sugar-Ps increased when phospholipids declined and poplar plants entering the vegetative growth period and, hence, metabolic activity increases. These results indicate that poplar trees adopt a policy of P nutrition without P storage and mobilization that is different from their N- and S-nutrition strategies.

Highlights

The annual growth cycle of temperate woody perennials is characterized by sequential periods of dormancy and active growth (Shim et al, 2014)
In twig bark and wood, the C level was similar throughout the annual growth cycle, whereas the N level was highest during dormancy and in early spring before bud break (Figures 1C–F)
The metabolite and lipid profile of poplar twig organs/tissues showed seasonal and tissue specific differences that can be linked to C, N, and S storage and mobilization processes and support the lack on any P storage

Summary

Introduction

The annual growth cycle of temperate woody perennials is characterized by sequential periods of dormancy and active growth (Shim et al, 2014). A detailed view of the poplar annual growth cycle has been presented by Jansson and Douglas (2007) and Rohde and Bhalerao (2007). After growth cessation in late summer, buds, which break in the following spring, start to develop. Day length perception via the phytochrome system (Coleman et al, 1991; Shim et al, 2014), temperature control of gene expression (Sjödin et al, 2008; Rennenberg et al, 2010; Wingler, 2015), endogenous control by chromatin remodeling, DNA and histone modification via methylation and acetylation (Karlberg et al, 2010; Conde et al, 2013; Shim et al, 2014), modulation of transcription factors (Ko et al, 2011) and phytohormones (Rohde and Bhalerao, 2007; Karlberg et al, 2010; Wingler, 2015) have been described to control the switch from dormancy to active growth and vice versa

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