Evolution of the Crop Rhizosphere: Impact of Domestication on Root Exudates in Tetraploid Wheat (Triticum turgidum L.)

Iannucci, Anna; Fragasso, Mariagiovanna; Beleggia, Romina; Nigro, Federica; Papa, Roberto

doi:10.3389/fpls.2017.02124

Cited by 95 publications

(92 citation statements)

References 39 publications

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“…The metabolites detected in B. distachyon root exudates in this study (Table S3) were comparable to metabolites detected in exudates of other grasses such as wheat (Iannucci et al , 2017), maize (Carvalhais et al , 2011), rice (Bacilio-Jiménez et al , 2003), Avena barbata (Zhalnina et al , 2018) and dicots such as Arabidopsis (Chaparro et al , 2013). Similarly, the B. distachyon exudation profile varied with developmental stage, as reported for other plants (Fig.…”

Section: Discussionsupporting

confidence: 76%

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Multi-lab EcoFAB study shows highly reproducible physiology and depletion of soil metabolites by a model grass

Sasse

Kant

Cole

et al. 2018

Preprint

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There is a dynamic reciprocity between plants and their environment: On one hand, the physiochemical properties of soil influence plant morphology and metabolism, while on the other, root morphology and exudates shape the environment surrounding roots. Here, we investigate both of these aspects as well as the reproducibility of these responses across laboratories. The model grass Brachypodium distachyon was grown in phosphate-sufficient and phosphate-deficient mineral media, as well as in sterile soil extract, within fabricated ecosystem (EcoFAB) devices across four laboratories. Tissue weight and phosphate content, total root length, root tissue and exudate metabolic profiles were found to be consistent across laboratories and distinct between experimental treatments. Plants grown in soil extract were morphologically and metabolically distinct in all laboratories, with root hairs four times longer compared to other growth conditions. Further, plants depleted half of the investigated metabolites from the soil extract. To interact with their environment, plants not only adapt morphology and release complex metabolite mixtures; they also selectively deplete a range of soil-derived metabolites. The EcoFABs utilized here generated high inter-laboratory reproducibility, demonstrating that their value in standardized investigations of plant traits.

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Section: Discussionsupporting

confidence: 76%

“…S2). Interestingly, altered root:shoot ratios were recently also detected for wheat genotypes grown in different soils (Iannucci et al , 2017), suggesting that different soils might affect root:shoot ratio and possibly also metabolic profiles in different ways.…”

Section: Discussionmentioning

confidence: 99%

Multi-lab EcoFAB study shows highly reproducible physiology and depletion of soil metabolites by a model grass

Sasse

Kant

Cole

et al. 2018

Preprint

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“…This prevents stem lodging that arose in response to the increase in size and biomass of the spike, because of the massive fertilization of fields implemented after the Second World War (Berry et al, 2015;Borojevic & Borojevic, 2005). Modern genotypes may differ from ancient genotypes in terms of metabolic composition (Di Loreto et al, 2018;Gotti et al, 2018;Iannucci, Fragasso, Beleggia, Nigro, & Papa, 2017;Shaposhnikov et al, 2016) and root architecture (Beyer et al, 2018;Horst, Abdou, & Wiesler, 1993;Pour-Aboughadareh, Ahmadi, Mehrabi, Moghaddam, & Etminan, 2017;Shaposhnikov et al, 2016;Siddique et al, 1990), which is likely to affect plant × PGPR interactions. Against this background, however, results also revealed that (a) many ancient genotypes were not effective for interaction (especially colonization) with P. kilonensis F113, whereas (b) interaction effectiveness with F113 had been maintained in a significant proportion of modern wheat genotypes.…”

Section: Discussionmentioning

confidence: 99%

Ancient wheat varieties have a higher ability to interact with plant growth‐promoting rhizobacteria

Valente

Gerin

Gouis

et al. 2019

Plant Cell & Environment

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Plant interactions with plant growth‐promoting rhizobacteria (PGPR) are highly dependent on plant genotype. Modern plant breeding has largely sought to improve crop performance but with little focus on the optimization of plant × PGPR interactions. The interactions of the model PGPR strain Pseudomonas kilonensis F113 were therefore compared in 199 ancient and modern wheat genotypes. A reporter system, in which F113 colonization and expression of 2,4‐diacetylphloroglucinol biosynthetic genes (phl) were measured on roots was used to quantify F113 × wheat interactions under gnotobiotic conditions. Thereafter, eight wheat accessions that differed in their ability to interact with F113 were inoculated with F113 and grown in greenhouse in the absence or presence of stress. F113 colonization was linked to improved stress tolerance. Moreover, F113 colonization and phl expression were higher overall on ancient genotypes than modern genotypes. F113 colonization improved wheat performance in the four genotypes that showed the highest level of phl expression compared with the four genotypes in which phl expression was lowest. Taken together, these data suggest that recent wheat breeding strategies have had a negative impact on the ability of the plants to interact with PGPR.

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“…pesticides, fertilizer), influence the below-ground diversity and function of soil microbes (Vries & Wallenstein, 2017), however, it is less clear if crops themselves cultivate different below-ground interactions compared to their wild relatives. Crops have reduced genetic diversity, which could influence the type, strength or diversity of interactions experienced belowground (Pérez-Jaramillo et al, 2016), and differences in root architecture (Schmidt, Bowles, & Gaudin, 2016) and root exudates (Iannucci, Fragasso, Beleggia, Nigro, & Papa, 2017) among crops and wild relatives can be pronounced. Yet, it is totally unknown whether domestication-mediated differences in rhizosphere microbes have functional consequences in the context of plant-soil feedback.…”

Section: Introductionmentioning

confidence: 99%

Domesticated tomatoes are more vulnerable to negative plant–soil feedbacks than their wild relatives

Carrillo

Ingwell

et al. 2019

Journal of Ecology

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Domesticated plants can differ from their wild counterparts in the strength and outcome of species interactions, both above‐ and belowground. Plant–soil feedbacks influence plant success, and plant‐associated soil microbial communities can influence plant interactions with herbivores and their natural enemies, yet, it remains unclear if domestication has changed these relationships. To determine the effects of domestication on plant–soil interactions, we characterized soil microbial communities associated with various cultivars of domesticated tomato and some of its wild relatives. We measured the strength and direction of plant–soil feedbacks for domesticated and wild tomatoes, and the effects of soil on plant resistance to specialist herbivory by Manduca sexta, and the attraction of a parasitoid wasp, Cotesia congregata. Domesticated tomatoes and their wild relatives had negative plant–soil feedbacks, as conspecifics cultivated soil that negatively impacted performance of subsequent plants (longer germination time, lower biomass) than if they grew in non‐tomato soils. Significant variation existed among domesticated and wild tomato varieties in the strength of these feedbacks, ranging from neutral to strongly negative. For above‐ground plant biomass, tomato wild relatives were unaffected by growing in tomato‐conditioned soil, whereas domesticated tomatoes grew smaller in tomato soil, indicating effects of plant domestication. Overall, increased microbial biomass within the rhizosphere resulted in progressively less‐negative plant–soil feedbacks. Plant cultivars had different levels of resistance to herbivory by M. sexta, but this did not depend on plant domestication or soil type. The parasitoid C. congregata was primarily attracted to herbivore damaged plants, independent of plant domestication status, and for these damaged plants, wasps preferred some cultivars over others, and wild plants grown in tomato soil over wild plants grown in non‐tomato soil. Synthesis. These results indicate that crop tomatoes are more likely to show negative plant–soil feedbacks than wild progenitors, which could partially explain their sensitivity to monocultures in agricultural soils. Furthermore, cultivar‐specific variation in the ability to generate soil microbial biomass, independent of domestication status, appears to buffer the negative consequences of sharing the same soil. Last, soil legacies were relatively absent for herbivores, but not for parasitoid wasps, suggesting trophic level specificity in soil feedbacks on plant–insect interactions.

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Evolution of the Crop Rhizosphere: Impact of Domestication on Root Exudates in Tetraploid Wheat (Triticum turgidum L.)

Cited by 95 publications

References 39 publications

Multi-lab EcoFAB study shows highly reproducible physiology and depletion of soil metabolites by a model grass

Multi-lab EcoFAB study shows highly reproducible physiology and depletion of soil metabolites by a model grass

Ancient wheat varieties have a higher ability to interact with plant growth‐promoting rhizobacteria

Domesticated tomatoes are more vulnerable to negative plant–soil feedbacks than their wild relatives

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