Strigolactone Levels in Dicot Roots Are Determined by an Ancestral Symbiosis-Regulated Clade of the PHYTOENE SYNTHASE Gene Family.

Ron Stauder,Wouter Kohlen,Gerd U Balcke,Michael H Walter,Ralf Welsch,Maurizio Camagna,Alain Tissier

doi:10.3389/fpls.2018.00255

Abstract

Strigolactones (SLs) are apocarotenoid phytohormones synthesized from carotenoid precursors. They are produced most abundantly in roots for exudation into the rhizosphere to cope with mineral nutrient starvation through support of root symbionts. Abscisic acid (ABA) is another apocarotenoid phytohormone synthesized in roots, which is involved in responses to abiotic stress. Typically low carotenoid levels in roots raise the issue of precursor supply for the biosynthesis of these two apocarotenoids in this organ. Increased ABA levels upon abiotic stress in Poaceae roots are known to be supported by a particular isoform of phytoene synthase (PSY), catalyzing the rate-limiting step in carotenogenesis. Here we report on novel PSY3 isogenes from Medicago truncatula (MtPSY3) and Solanum lycopersicum (SlPSY3) strongly expressed exclusively upon root interaction with symbiotic arbuscular mycorrhizal (AM) fungi and moderately in response to phosphate starvation. They belong to a widespread clade of conserved PSYs restricted to dicots (dPSY3) distinct from the Poaceae-PSY3s involved in ABA formation. An ancient origin of dPSY3s and a potential co-evolution with the AM symbiosis is discussed in the context of PSY evolution. Knockdown of MtPSY3 in hairy roots of M. truncatula strongly reduced SL and AM-induced C13 α-ionol/C14 mycorradicin apocarotenoids. Inhibition of the reaction subsequent to phytoene synthesis revealed strongly elevated levels of phytoene indicating induced flux through the carotenoid pathway in roots upon mycorrhization. dPSY3 isogenes are coregulated with upstream isogenes and downstream carotenoid cleavage steps toward SLs (D27, CCD7, CCD8) suggesting a combined carotenoid/apocarotenoid pathway, which provides “just in time”-delivery of precursors for apocarotenoid formation.

Highlights

Strigolactones (SLs) and abscisic acid (ABA) are carotenoid-derived phytohormones synthesized through enzymatic oxidative tailoring of carotenoid precursors (Walter and Strack, 2011; McQuinn et al, 2015; Nisar et al, 2015; Hou et al, 2016)
Based on existing annotations we propose to name this cladedicot PSY3 to distinguish it from the PSY3 of the Poaceae to which it is phylogenetically distinct (Figure 4 and Supplementary Figure S5). dPSY3-type genes were recognized previously in several studies (Arango et al, 2010; Peng et al, 2013; Fu et al, 2014; Ampomah-Dwamena et al, 2015) but no major developmental or environmental stimulus for their transcriptional activation was reported far except for low expression confined to roots in melon (Qin et al, 2011) and tomato (Fantini et al, 2013)
The report of root colonization by arbuscular mycorrhizal (AM) fungi as a single strong cue for transcriptional activation of dPSY3 genes is one major novelty of this paper

Summary

Introduction

Strigolactones (SLs) and abscisic acid (ABA) are carotenoid-derived phytohormones (apocarotenoids) synthesized through enzymatic oxidative tailoring of carotenoid precursors (Walter and Strack, 2011; McQuinn et al, 2015; Nisar et al, 2015; Hou et al, 2016). They are most abundantly formed in roots but are synthesized in other organs. Further modifications of the carlactone intermediate involve one or more oxidative steps by P450 enzymes called MAX1 leading to canonical and non-canonicals SLs (Figure 1; Alder et al, 2012; Al-Babili and Bouwmeester, 2015). The ABA precursor xanthoxin results from a single cleavage reaction on an epoxidized 9-cis-zeaxanthin isomer (Figure 1; Nambara and Marion-Poll, 2005)

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Conclusion