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Interplant communication of tomato plants through underground common mycorrhizal networks.

ABSTRACT: Plants can defend themselves to pathogen and herbivore attack by responding to chemical signals that are emitted by attacked plants. It is well established that such signals can be transferred through the air. In theory, plants can also communicate with each other through underground common mycorrhizal networks (CMNs) that interconnect roots of multiple plants. However, until now research focused on plant-to-plant carbon nutrient movement and there is no evidence that defense signals can be exchanged through such mycorrhizal hyphal networks. Here, we show that CMNs mediate plant-plant communication between healthy plants and pathogen-infected tomato plants (Lycopersicon esculentum Mill.). After establishment of CMNs with the arbuscular mycorrhizal fungus Glomus mosseae between tomato plants, inoculation of 'donor' plants with the pathogen Alternaria solani led to increases in disease resistance and activities of the putative defensive enzymes, peroxidase, polyphenol oxidase, chitinase, ?-1,3-glucanase, phenylalanine ammonia-lyase and lipoxygenase in healthy neighbouring 'receiver' plants. The uninfected 'receiver' plants also activated six defence-related genes when CMNs connected 'donor' plants challenged with A. solani. This finding indicates that CMNs may function as a plant-plant underground communication conduit whereby disease resistance and induced defence signals can be transferred between the healthy and pathogen-infected neighbouring plants, suggesting that plants can 'eavesdrop' on defence signals from the pathogen-challenged neighbours through CMNs to activate defences before being attacked themselves.

SUBMITTER: Song YY

PROVIDER: S-EPMC2954164 | biostudies-literature | 2010 Oct

REPOSITORIES: biostudies-literature

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Interplant communication of tomato plants through underground common mycorrhizal networks.

Song Yuan Yuan YY Zeng Ren Sen RS Xu Jian Feng JF Li Jun J Shen Xiang X Yihdego Woldemariam Gebrehiwot WG

PloS one 20101013 10

Plants can defend themselves to pathogen and herbivore attack by responding to chemical signals that are emitted by attacked plants. It is well established that such signals can be transferred through the air. In theory, plants can also communicate with each other through underground common mycorrhizal networks (CMNs) that interconnect roots of multiple plants. However, until now research focused on plant-to-plant carbon nutrient movement and there is no evidence that defense signals can be exch ...[more]

PMID: 20967206

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Project description:Common mycorrhizal networks (CMNs) allow the transfer of nutrients between plants, influencing the growth of the neighboring plants and soil properties. Cleistogene squarrosa (C. squarrosa) is one of the most common grass species in the steppe ecosystem of Inner Mongolia, where nitrogen (N) is often a key limiting nutrient for plant growth, but little is known about whether CMNs exist between neighboring individuals of C. squarrosa or play any roles in the N acquisition of the C. squarrosa population. In this study, two C. squarrosa individuals, one as a donor plant and the other as a recipient plant, were planted in separate compartments in a partitioned root-box. Adjacent compartments were separated by 37 µm nylon mesh, in which mycorrhizal hyphae can go through but not roots. The donor plant was inoculated with arbuscular mycorrhizal (AM) fungi, and their hyphae potentially passed through nylon mesh to colonize the roots of the recipient plant, resulting in the establishment of CMNs. The formation of CMNs was verified by microscopic examination and 15N tracer techniques. Moreover, different levels of N fertilization (N0 = 0, N1 = 7.06, N2 = 14.15, N3 = 21.19 mg/kg) were applied to evaluate the CMNs' functioning under different soil nutrient conditions. Our results showed that when C. squarrosa-C. squarrosa was the association, the extraradical mycelium transferred the 15N in the range of 45-55% at different N levels. Moreover, AM fungal colonization of the recipient plant by the extraradical hyphae from the donor plant significantly increased the plant biomass and the chlorophyll content in the recipient plant. The extraradical hyphae released the highest content of glomalin-related soil protein into the rhizosphere upon N2 treatment, and a significant positive correlation was found between hyphal length and glomalin-related soil proteins (GRSPs). GRSPs and soil organic carbon (SOC) were significantly correlated with mean weight diameter (MWD) and helped in the aggregation of soil particles, resulting in improved soil structure. In short, the formation of CMNs in this root-box experiment supposes the existence of CMNs in the typical steppe plants, and CMNs-mediated N transfer and root colonization increased the plant growth and soil properties of the recipient plant.

Project description:The worldwide use of plant biostimulants (PBs) represents an environmentally friendly tool to increase crop yield and productivity. PBs include different substances, compounds, and growth-promoting microorganism formulations, such as those derived from arbuscular mycorrhizal fungi (AMF) or seaweed extracts (SEs), which are used to regulate or enhance physiological processes in plants. This study analyzed the physiological, ecological, and biochemical implications of the addition of two PBs, AMF or SE (both alone and in combination), on tomato plants (Solanum lycopersicum L. cv. "Rio Fuego"). The physiological responses evaluated were related to plant growth and photosynthetic performance. The ecological benefits were assessed based on the success of AMF colonization, flowering, resistance capacity, nonphotochemical quenching (NPQ), and polyphenol content. Biochemical effects were evaluated via protein, lipid, carbohydrate, nitrogen, and phosphorous content. Each PB was found to benefit tomato plants in a different but complementary manner. AMF resulted in an energetically expensive (high ETRMAX but low growth) but protective (high NPQ and polyphenol content) response. AMF + nutritive solution (NS) induced early floration but resulted in low protein, carbohydrate, and lipid content. Both AMF and AMF + NS favored foliar instead of root development. In contrast, SE and SE + NS favored protein content and root development and did not promote flowering. However, the combination of both PBs (AMF + SE) resulted in an additive effect, reflected in an increase in both foliar and root growth as well as protein and carbohydrate content. Moreover, a synergistic effect was also found, which was expressed in accelerated flowering and AMF colonization. We present evidence of benefits to plant performance (additive and synergistic) due to the interactive effects between microbial (AMF) and nonmicrobial (SEs) PBs and propose that the complementary modes of action of both PBs may be responsible for the observed positive effects due to the new and emerging properties of their components instead of exclusively being the result of known constituents. These results will be an important contribution to biostimulant research and to the development of a second generation of PBs in which combined and complementary mechanisms may be functionally designed.

Dataset Information

Interplant communication of tomato plants through underground common mycorrhizal networks.

Publications

Interplant communication of tomato plants through underground common mycorrhizal networks.

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