Abstract

Common oak trees display endogenous rhythmic growth with alternating shoot and root flushes. To explore the mechanisms involved, microcuttings of the Quercus robur L. clone DF159 were used for (13)C/(15)N labelling in combination with RNA sequencing (RNASeq) transcript profiling of shoots and roots. The effect of plant internal resource availability on the rhythmic growth of the cuttings was tested through inoculation with the ectomycorrhizal fungus Piloderma croceum. Shoot and root flushes were related to parallel shifts in above- and below-ground C and, to a lesser extent, N allocation. Increased plant internal resource availability by P. croceum inoculation with enhanced plant growth affected neither the rhythmic growth nor the associated resource allocation patterns. Two shifts in transcript abundance were identified during root and shoot growth cessation, and most concerned genes were down-regulated. Inoculation with P. croceum suppressed these transcript shifts in roots, but not in shoots. To identify core processes governing the rhythmic growth, functions [Gene Ontology (GO) terms] of the genes differentially expressed during the growth cessation in both leaves and roots of non-inoculated plants and leaves of P. croceum-inoculated plants were examined. Besides genes related to resource acquisition and cell development, which might reflect rather than trigger rhythmic growth, genes involved in signalling and/or regulated by the circadian clock were identified. The results indicate that rhythmic growth involves dramatic oscillations in plant metabolism and gene regulation between below- and above-ground parts. Ectomycorrhizal symbiosis may play a previously unsuspected role in smoothing these oscillations without modifying the rhythmic growth pattern.

Highlights

  • The growth of many trees is not continuous, but is interrupted by episodic rest phases (Kuehny et al, 1997; McCown, 2000; Barthelemy and Caraglio, 2007)

  • Gene Ontology (GO) terms involved in C metabolism including ‘carbon utilization’ and ‘trehalose biosynthetic process’ were enriched, with 10 up-regulated trehalose 6-phosphate synthase contigs in Cont_LR

  • The apparent enhancement of local C utilization in roots probably counterbalances the reduction in carbohydrate transport to lateral root (LR) during root growth cessation (RGC) since the GO term ‘UDP-glucose transport’ was enriched in down-regulated contigs

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Summary

Introduction

The growth of many trees is not continuous, but is interrupted by episodic rest phases (Kuehny et al, 1997; McCown, 2000; Barthelemy and Caraglio, 2007). To assess the effects of variations in downward soluble sugar export during shoot flushes, Willaume and Pages (2011) ablated source leaves and cotyledons of Quercus pubescens seedlings. This reduced the concentrations of nonstructural carbohydrates in the seedlings’ root apices, and root growth. In young micropropagated apple trees, the growth of secondary roots rhythmically alternates with shoot flushes, in processes that Costes et al (2006) hypothesized may be governed by oscillations in downward carbohydrate transfer, and possibly oscillations of nitrogen (N) metabolism. The hypothesis of Costes et al (2006) that balanced shoot and root rhythmic development is governed by carbon (C) and by N partitioning has not yet been rigorously confirmed or refuted

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