Elsevier

Journal of Plant Physiology

Volume 168, Issue 3, 15 February 2011, Pages 294-297
Journal of Plant Physiology

Short communication
Arbuscular mycorrhizal symbiosis decreases strigolactone production in tomato

https://doi.org/10.1016/j.jplph.2010.08.011Get rights and content

Abstract

Strigolactones are a new class of plant hormones emerging as important signals in the control of plant architecture. In addition, they are key elements in plant communication with several rhizosphere organisms. Strigolactones are exuded into the soil, where they act as host detection signals for arbuscular mycorrhizal (AM) fungi, but also as germination stimulants for root parasitic plant seeds. Under phosphate limiting conditions, plants up-regulate the secretion of strigolactones into the rhizosphere to promote the formation of AM symbiosis. Using tomato as a model plant, we have recently shown that AM symbiosis induces changes in transcriptional and hormonal profiles. Using the same model system, here we analytically demonstrate, using liquid chromatography–tandem mass spectrometry, that strigolactone production is also significantly reduced upon AM symbiosis. Considering the dual role of the strigolactones in the rhizosphere as signals for AM fungi and parasitic plants, we discuss the potential implications of these changes in the plant interaction with both organisms.

Introduction

Arbuscular mycorrhizal (AM) symbiosis is a mutualistic association established between certain soil fungi and most terrestrial plants, and it is considered a key step in the evolution of aquatic into terrestrial plants (Parniske, 2008). During the symbiosis, AM fungi obtain carbohydrates from their host plant and, in return, the plants obtain water and mineral nutrients (mainly phosphorous and nitrogen) from their fungal partners. In addition to improving the nutritional status, the symbiosis enables the plant to perform better under stressful conditions (Pozo and Azcón-Aguilar, 2007, Parniske, 2008). AM symbiosis establishment and functioning requires a high degree of coordination between the two partners based on a finely regulated molecular dialogue that orchestrates the complex symbiotic program (Paszkowski, 2006, Hause et al., 2007, Requena et al., 2007). The chemical dialogue starts in the rhizosphere, before there is any contact between the partners. Strigolactones are exuded by the plant roots into the soil and act as host detection signals for the AM fungi, stimulating their metabolism and hyphal branching (Akiyama et al., 2005, Parniske, 2008). In the rhizosphere, the strigolactones are also germination stimulants for root parasitic plant seeds of the family Orobancheaceae, such as Striga, Orobanche and Phelipanche spp. (Bouwmeester et al., 2007). In accordance with their AM fungi attracting role, under low nutrient conditions (mainly phosphorous and nitrogen), plants produce more strigolactones (Yoneyama et al., 2007, López-Ráez et al., 2008a), but this also increases the risk that the plant is abused by the parasitic weeds to establish a parasitic interaction (Bouwmeester et al., 2007). Recently, strigolactones have also been recognized as a novel class of plant hormones because, in addition to their role as signaling molecules in the rhizosphere, they also control plant architecture signaling inhibition of shoot branching (Gómez-Roldán et al., 2008, Umehara et al., 2008). Other phytohormones, such as ethylene, salicylic acid, abscisic acid and jasmonates have been proposed to be important regulators in the mutualistic interaction between plants and AM fungi (Herrera-Medina et al., 2003, Hause et al., 2007, Herrera-Medina et al., 2007, Riedel et al., 2008). We have recently shown that AM symbiosis alters both hormonal and transcriptional profiles in tomato roots, especially the oxylipin pathway (López-Ráez et al., 2010). With respect to strigolactones, there are indications that regulation of their levels occurs in the host plant once the symbiosis has been established. It was shown that AM fungal inoculation of maize and sorghum led to a reduction of Striga hermonthica infection (Lendzemo et al., 2005), and it was proposed that this reduced infection was caused, at least partially, by a reduction in the production of strigolactones in the mycorrhizal plants (Lendzemo et al., 2007, Sun et al., 2008), although no analytical evidence was provided. In the present work, a reduction in strigolactone production during AM symbiosis is also shown in tomato plants, indicating a conserved response in dicotyledonous and monocotyledonous plant species. Moreover, the reduction in strigolactones by AM symbiosis is, for the first time, analytically demonstrated by liquid chromatography–tandem mass spectrometry (LC–MS/MS). The potential use of AM fungi as a sustainable alternative in programs for parasitic weed control is discussed.

Section snippets

Plant growth and AM fungal inoculation

Tomato seedlings (Solanum lycopersicum L. cv. BetterBoy) were grown in pots with a sterile sand:soil (4:1) mixture and inoculated or not with a 10% (v:v) soil-sand-based inoculum containing Glomus mosseae (BEG12) or Glomus intraradices (BEG 121) propagules. Five plants per treatment were used. Plants were randomly distributed and grown in a greenhouse and watered three times a week with Long Ashton nutrient solution (Hewitt, 1966) containing 25% of the standard phosphorous concentration (

Germination stimulatory activity of root exudates from AM fungi-colonized tomato plants

The regulation of strigolactone production during AM symbiosis was assayed using tomato plants and two different AM fungi. In the case of G. intraradices, the percentage of colonized roots reached 75% after eight weeks of growth, whereas G. mosseae colonized only about 5% of the roots in this experiment. Strigolactone levels in root exudates from mycorrhizal and non-mycorrhizal plants were estimated using a germination bioassay for P. ramosa seeds (López-Ráez et al., 2008a). A clear reduction

Acknowledgments

This work was supported by grants AGL2006-08029 and AGL2009-07691 from the National R&D Plan of the MINCIN, PERG-02-2007-224751 from the Marie Curie program from the European Commission and The Netherlands Organization for Scientific Research (NWO; VICI-grant to HB). JAL-R is supported by a postdoctoral contract (JAE-Doc) from the CSIC and IF by a PhD fellowship from the MINCIN. We thank Juan M. García and Ana Jiménez for excellent technical assistance.

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