Root-to-shoot signalling in mycorrhizal tomato plants upon Botrytis cinerea infection

Sanmartín, Neus; Sánchez-Bel, Paloma; Pastor, Victoria; Pastor-Fernández, Julia; Mateu, Diego; Pozo, Marı́a J.; Cerezo, Miguel; Flors, Víctor

doi:10.1016/j.plantsci.2020.110595

Cited by 35 publications

(33 citation statements)

References 63 publications

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“…A strongest defensive capacity in AM plants has been shown in previous studies, usually through phytohormone measurements or quantification of metabolites with known toxic effects against insects ( Andrade et al , 2013 ; Song et al , 2013 ; Minton et al , 2016 ; Tomczak et al , 2016 ; Sanmartín et al , 2020b ). However, a more holistic overview of the possible modulation of metabolism in the host plant is missing.…”

Section: Discussionmentioning

confidence: 82%

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Mycorrhizal symbiosis primes the accumulation of antiherbivore compounds and enhances herbivore mortality in tomato

Rivero

Lidoy

Llopis-Giménez

et al. 2021

Journal of Experimental Botany

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Plant association with arbuscular mycorrhizal fungi (AMF) can increase their ability to overcome multiple stresses, but their impact on plant interactions with herbivorous insects is controversial. Here we show higher mortality of the leaf-chewer Spodoptera exigua when fed on tomato plants colonized by the AMF Funneliformis mosseae, evidencing mycorrhiza-induced resistance. In search of the underlying mechanisms, an untargeted metabolomic analysis through ultra-performance liquid chromatography tandem mass spectrometry (UPLC-MS) was performed. The results showed that mycorrhizal symbiosis had a very limited impact on the leaf metabolome in the absence of stress, but significantly modulated the response to herbivory in the damaged area. A cluster of over accumulated metabolites was identified in those leaflets damaged by S. exigua feeding in mycorrhizal plants, while unwounded distal leaflets responded similar to those from non-mycorrhizal plants. These primed-compounds were mostly related to alkaloids, fatty acid derivatives and phenylpropanoid-polyamine conjugates. The deleterious effect on larval survival of some of these compounds, including the alkaloid physostigmine, the fatty acid derivatives 4-oxododecanedioic acid and azelaic acid, was confirmed. Thus, our results evidence the impact of AMF on metabolic reprograming upon herbivory that leads to a primed accumulation of defensive compounds.

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Section: Discussionmentioning

confidence: 82%

“…In previous studies, we showed that AMF colonization resulted in a strong metabolic rearrangement in tomato plant roots in absence of stress ( Rivero et al , 2015 ; 2018 , Sanmartín et al , 2020b ). Here, we found a minimal alteration of the metabolome in aboveground tissues.…”

Section: Discussionmentioning

confidence: 99%

Mycorrhizal symbiosis primes the accumulation of antiherbivore compounds and enhances herbivore mortality in tomato

Rivero

Lidoy

Llopis-Giménez

et al. 2021

Journal of Experimental Botany

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“…In fact, AM enhances plant phenotypic plasticity, an important advantage in heterogeneous and changing environments where the precise allocation of limited resources between growth and stress resistance is critical for survival [ 15 , 16 , 17 ]. Mycorrhizal plants are usually more resistant to abiotic stresses such as drought, salinity, and heavy metal pollution [ 17 , 18 , 19 ], but AMF can also increase plant resistance/tolerance to biotic stresses by triggering the so-called mycorrhiza-induced resistance (MIR) against diverse root and foliar pathogens and pests [ 20 , 21 , 22 , 23 , 24 , 25 , 26 , 27 , 28 ]. In return, AMF require photosynthates and lipids from the plant to complete their life cycle.…”

Section: Introductionmentioning

confidence: 99%

“…Under favorable conditions, Botrytis conidia in the soil and in infected plant debris rapidly germinates and can colonize lettuce stems and leaves [ 54 ]. Remarkably, mycorrhizal colonization has been shown to reduce Botrytis proliferation and damage in tomatoes, another relevant crop [ 23 , 25 , 26 , 55 ]. In previous studies, mycorrhizal colonization was shown to improve lettuce nutritional content and enhanced abiotic stress tolerance [ 18 , 56 , 57 , 58 , 59 ], but some of those benefits depended on the crop management or conditions [ 56 , 57 ].…”

Section: Introductionmentioning

confidence: 99%

Mycorrhiza-Induced Resistance against Foliar Pathogens Is Uncoupled of Nutritional Effects under Different Light Intensities

Hoz

Rivero

Azcón‐Aguilar

et al. 2021

JoF

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The use of microbial inoculants, particularly arbuscular mycorrhizal fungi, has great potential for sustainable crop management, which aims to reduce the use of chemical fertilizers and pesticides. However, one of the major challenges of their use in agriculture is the variability of the inoculation effects in the field, partly because of the varying environmental conditions. Light intensity and quality affect plant growth and defense, but little is known about their impacts on the benefits of mycorrhizal symbioses. We tested the effects of five different light intensities on plant nutrition and resistance to the necrotrophic foliar pathogen Botrytis cinerea in mycorrhizal and non-mycorrhizal lettuce plants. Our results evidence that mycorrhiza establishment is strongly influenced by light intensity, both regarding the extension of root colonization and the abundance of fungal vesicles within the roots. Light intensity also had significant effects on plant growth, nutrient content, and resistance to the pathogen. The effect of the mycorrhizal symbiosis on plant growth and nutrient content depended on the light intensity, and mycorrhiza efficiently reduced disease incidence and severity under all light intensities. Thus, mycorrhiza-induced resistance can be uncoupled from mycorrhizal effects on plant nutrition. Therefore, mycorrhizal symbioses can be beneficial by providing biotic stress protection even in the absence of nutritional or growth benefits.

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“…Lignans accumulated only in roots both as a local or systemic response and have been recently related to plant defence. Overexpression of a lignan biosynthesis gene in soybean roots induced resistance against the oomycete Phytophthora sojae (Li et al, 2017), and we have recently shown that the root derived lignan yatein is involved in mycorrhiza induced resistance against B. cinerea in tomato (Sanmartín et al, 2020). In contrast to lignans, flavonoids accumulated in roots only as a local response to OGs, and in leaves as both local and systemic response to leaf treatment.…”

Section: Discussionmentioning

confidence: 99%

Roots drive oligogalacturonide‐induced systemic immunity in tomato

Gamir

Minchev

Berrio

et al. 2020

Plant Cell & Environment

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Oligogalacturonides (OGs) are fragments of pectin released from the plant cell wall during insect or pathogen attack. They can be perceived by the plant as damage signals, triggering local and systemic defence responses. Here, we analyse the dynamics of local and systemic responses to OG perception in tomato roots or shoots, exploring their impact across the plant and their relevance in pathogen resistance. Targeted and untargeted metabolomics and gene expression analysis in plants treated with purified OGs revealed that local responses were transient, while distal responses were stronger and more sustained. Remarkably, changes were more conspicuous in roots, even upon foliar application of the OGs. The treatments differentially activated the synthesis of defence-related hormones and secondary metabolites including flavonoids, alkaloids and lignans, some of them exclusively synthetized in roots. Finally, the biological relevance of the systemic defence responses activated upon OG perception was confirmed, as the treatment induced systemic resistance to Botrytis cinerea. Overall, this study shows the differential regulation of tomato defences upon OGs perception in roots and shoots and reveals the key role of roots in the coordination of the plant responses to damage sensing.

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Root-to-shoot signalling in mycorrhizal tomato plants upon Botrytis cinerea infection

Cited by 35 publications

References 63 publications

Mycorrhizal symbiosis primes the accumulation of antiherbivore compounds and enhances herbivore mortality in tomato

Mycorrhizal symbiosis primes the accumulation of antiherbivore compounds and enhances herbivore mortality in tomato

Mycorrhiza-Induced Resistance against Foliar Pathogens Is Uncoupled of Nutritional Effects under Different Light Intensities

Roots drive oligogalacturonide‐induced systemic immunity in tomato

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