Abstract

The apocarotenoid zaxinone promotes growth and suppresses strigolactone biosynthesis in rice. To shed light on the mechanisms underlying its growth-promoting effect, we employed a combined omics approach integrating transcriptomics and metabolomics analysis of rice seedlings treated with zaxinone, and determined the resulting changes at the cellular and hormonal levels. Metabolites as well as transcripts analysis demonstrate that zaxinone application increased sugar content and triggered glycolysis, the tricarboxylic acid cycle and other sugar-related metabolic processes in rice roots. In addition, zaxinone treatment led to an increased root starch content and induced glycosylation of cytokinins. The transcriptomic, metabolic and hormonal changes were accompanied by striking alterations of roots at cellular level, which showed an increase in apex length, diameter, and the number of cells and cortex cell layers. Remarkably, zaxinone did not affect the metabolism of roots in a strigolactone deficient mutant, suggesting an essential role of strigolactone in the zaxinone growth-promoting activity. Taken together, our results unravel zaxinone as a global regulator of the transcriptome and metabolome, as well as of hormonal and cellular composition of rice roots. Moreover, they suggest that zaxinone promotes rice growth most likely by increasing sugar uptake and metabolism, and reinforce the potential of this compound in increasing rice performance.

Highlights

  • The apocarotenoid zaxinone promotes growth and suppresses strigolactone biosynthesis in rice

  • We observed a significant increase in the levels of the major sugars sucrose, glucose, and fructose at 2 and 6 h after application of zaxinone, which was followed by a sharp decrease at 24 h

  • Many other primary metabolites, including several sugars, tricarboxylic acid (TCA) intermediates, and free amino acids, showed an increase only at the late, 24 h, time point (Fig. 1d and Supplementary Figs. 2b, 4). These results suggest that zaxinone application to roots in hydroponically grown seedlings causes a rapid global change in the primary metabolism of roots and, with a slight delay, in shoots

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Summary

Introduction

The apocarotenoid zaxinone promotes growth and suppresses strigolactone biosynthesis in rice. Our results unravel zaxinone as a global regulator of the transcriptome and metabolome, as well as of hormonal and cellular composition of rice roots They suggest that zaxinone promotes rice growth most likely by increasing sugar uptake and metabolism, and reinforce the potential of this compound in increasing rice performance. Carotenoids are widespread pigments fulfilling vital functions in plants, by protecting the photosynthetic apparatus from photo-oxidation and harnessing light energy[1] They are the precursor of a structurally diverse set of metabolites, generally called apocarotenoids, which include volatiles, colorants, signaling/regulatory molecules, and hormones. Metabolism is a central process required for the uptake and utilization of energy and nutrients to ensure the survival, reproduction, growth, and development of living organisms[16] Primary metabolites such as sugars, amino acids, nucleotides, organic acids, and fatty acids are essential for maintaining cellular homeostasis and for organismal life[17]. For instance sugars, such as sucrose, interact with different plant hormones and regulate bud development and shoot branching by modulating the signaling of auxin and SLs12,19,20

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