Network Analysis: A Systems Framework to Address Grand Challenges in Plant Pathology

Garrett, Karen A.; Alcalá-Briseño, Ricardo I.; Andersen, Kelsey F.; Buddenhagen, Christopher E.; Choudhury, Robin A.; Fulton, James C.; Nopsa, John Fredy Hernández; Poudel, Ravin; Xing, Yao‐Wu

doi:10.1146/annurev-phyto-080516-035326

Cited by 61 publications

(54 citation statements)

References 166 publications

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“…We also identified microbes specific to rootstock treatments. Further study of select microbes could help to identify candidate taxa for synthetic communities and support exploration of other layers of microbial information in associationbased single and multilayer networks (98). In the long term, identifying specific plant alleles/genes that correlate with target microbial taxa can inform plant breeding to meet goals beyond fruit traits and yield, perhaps including means to facilitate low-input sustainable agriculture through plant-mediated selection of desirable microbiome components.…”

Section: Discussionmentioning

confidence: 99%

Rootstocks Shape the Rhizobiome: Rhizosphere and Endosphere Bacterial Communities in the Grafted Tomato System

Poudel

Jumpponen

Kennelly

et al. 2019

Appl Environ Microbiol

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Root-associated microbes are critical to plant health and performance, although understanding of the factors that structure these microbial communities and the theory to predict microbial assemblages are still limited. Here, we use a grafted tomato system to study the effects of rootstock genotypes and grafting in endosphere and rhizosphere microbiomes that were evaluated by sequencing 16S rRNA. We compared the microbiomes of nongrafted tomato cultivar BHN589, selfgrafted BHN589, and BHN589 grafted to Maxifort or RST-04-106 hybrid rootstocks. Operational taxonomic unit (OTU)-based bacterial diversity was greater in Maxifort compared to the nongrafted control, whereas bacterial diversity in the controls (selfgrafted and nongrafted) and the other rootstock (RST-04-106) was similar. Grafting itself did not affect bacterial diversity; diversity in the self-graft was similar to that of the nongraft. Bacterial diversity was higher in the rhizosphere than in the endosphere for all treatments. However, despite the lower overall diversity, there was a greater number of differentially abundant OTUs (DAOTUs) in the endosphere, with the greatest number of DAOTUs associated with Maxifort. In a permutational multivariate analysis of variance (PERMANOVA), there was evidence for an effect of rootstock genotype on bacterial communities. The endosphere-rhizosphere compartment and study site explained a high percentage of the differences among bacterial communities. Further analyses identified OTUs responsive to rootstock genotypes in both the endosphere and rhizosphere. Our findings highlight the effects of rootstocks on bacterial diversity and composition. The influence of rootstock and plant compartment on microbial communities indicates opportunities for the development of designer communities and microbiome-based breeding to improve future crop production. IMPORTANCE Understanding factors that control microbial communities is essential for designing and supporting microbiome-based agriculture. In this study, we used a grafted tomato system to study the effect of rootstock genotypes and grafting on bacterial communities colonizing the endosphere and rhizosphere. To compare the bacterial communities in control treatments (nongrafted and self-grafted plants) with the hybrid rootstocks used by farmers, we evaluated the effect of rootstocks on overall bacterial diversity and composition. These findings indicate the potential for using plant genotype to indirectly select bacterial taxa. In addition, we identify taxa responsive to each rootstock treatment, which may represent candidate taxa useful for biocontrol and in biofertilizers.Citation Poudel R, Jumpponen A, Kennelly MM, Rivard CL, Gomez-Montano L, Garrett KA. 2019. Rootstocks shape the rhizobiome: rhizosphere and endosphere bacterial communities in the grafted tomato system. Appl Environ Microbiol 85:e01765-18. https://

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Section: Discussionmentioning

confidence: 99%

Rootstocks Shape the Rhizobiome: Rhizosphere and Endosphere Bacterial Communities in the Grafted Tomato System

Poudel

Jumpponen

Kennelly

et al. 2019

Appl Environ Microbiol

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“…Viral metagenomics approaches support the discovery of a large number of virus species in wild plants, crops, and vectors (22)(23)(24)(25). In addition to analyses of diversity indices, methods for evaluating associations among pathogens are needed to understand the potentially complex network of interactions among microbes, epidemiological dynamics, and bipartite networks specific to hostvector and plant-virus interactions (26,27). Network analysis provides insights into biological relationships in viral communities and can generate hypotheses about mechanisms that promote and prevent the cooccurrence of viruses in communities (28).…”

mentioning

confidence: 99%

Network Analysis of the Papaya Orchard Virome from Two Agroecological Regions of Chiapas, Mexico

Alcalá-Briseño

Casarrubias-Castillo²,

López-Ley³

et al. 2020

mSystems

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The study of complex ecological interactions, such as those among host, pathogen, and vector communities, can help to explain host ranges and the emergence of novel pathogens. We evaluated the viromes of papaya orchards, including weed and insect viromes, to identify common viruses in intensive production of papaya in the Pacific Coastal Plain and the Central Depression of Chiapas, Mexico. Samples of papaya cultivar Maradol, susceptible to papaya ringspot virus (PRSV), were categorized by symptoms by local farmers (papaya ringspot symptoms, non-PRSV symptoms, or asymptomatic). These analyses revealed the presence of 61 viruses, where only 4 species were shared among both regions, 16 showed homology to known viruses, and 36 were homologous with genera including Potyvirus, Comovirus, and Tombusvirus (RNA viruses) and Begomovirus and Mastrevirus (DNA viruses). We analyzed the network of associations between viruses and host-location combinations, revealing ecological properties of the network, such as an asymmetric nested pattern, and compared the observed network to null models of network association. Understanding the network structure informs management strategies, for example, revealing the potential role of PRSV in asymptomatic papaya and that weeds may be an important pathogen reservoir. We identify three key management implications: (i) each region may need a customized management strategy; (ii) visual assessment of papaya may be insufficient for PRSV, requiring diagnostic assays; and (iii) weed control within orchards may reduce the risk of virus spread to papaya. Network analysis advances understanding of host-pathogen interactions in the agroecological landscape. IMPORTANCE Virus-virus interactions in plants can modify host symptoms. As a result, disease management strategies may be unsuccessful if they are based solely on visual assessment and diagnostic assays for known individual viruses. Papaya ringspot virus is an important limiting factor for papaya production and likely has interactions with other viruses that are not yet known. Using high-throughput sequencing, we recovered known and novel RNA and DNA viruses from papaya orchards in Chiapas, Mexico, and categorized them by host and, in the case of papaya, symptom type: asymptomatic papaya, papaya with ringspot virus symptoms, papaya with nonringspot symptoms, weeds, and insects. Using network analysis, we demonstrated virus associations within and among host types and described the ecological community patterns. Recovery of viruses from weeds and asymptomatic papaya suggests the need for additional management attention. These analyses contribute to the understanding of the community structure of viruses in the agroecological landscape.

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“…A general measure such as the CCRI can usefully become a standard feature of PRAs, as a starting point in addressing a pest or disease for which there is limited information available. As more attention is focused on the invasive species and data collection increases, scenario analyses of management options, supported by epidemic simulation, could inform increasingly targeted surveillance and mitigation efforts (e.g., Garrett et al 2018 , Andersen et al 2019 ).…”

Section: Incorporating Cropland Connectivity In Risk Assessmentsmentioning

confidence: 99%

Global Cropland Connectivity: A Risk Factor for Invasion and Saturation by Emerging Pathogens and Pests

et al. 2020

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The geographic pattern of cropland is an important risk factor for invasion and saturation by crop-specific pathogens and arthropods. Understanding cropland networks supports smart pest sampling and mitigation strategies. We evaluate global networks of cropland connectivity for key vegetatively propagated crops (banana and plantain, cassava, potato, sweet potato, and yam) important for food security in the tropics. For each crop, potential movement between geographic location pairs was evaluated using a gravity model, with associated uncertainty quantification. The highly linked hub and bridge locations in cropland connectivity risk maps are likely priorities for surveillance and management, and for tracing intraregion movement of pathogens and pests. Important locations are identified beyond those locations that simply have high crop density. Cropland connectivity risk maps provide a new risk component for integration with other factors—such as climatic suitability, genetic resistance, and global trade routes—to inform pest risk assessment and mitigation.

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Network Analysis: A Systems Framework to Address Grand Challenges in Plant Pathology

Cited by 61 publications

References 166 publications

Rootstocks Shape the Rhizobiome: Rhizosphere and Endosphere Bacterial Communities in the Grafted Tomato System

Rootstocks Shape the Rhizobiome: Rhizosphere and Endosphere Bacterial Communities in the Grafted Tomato System

Network Analysis of the Papaya Orchard Virome from Two Agroecological Regions of Chiapas, Mexico

Global Cropland Connectivity: A Risk Factor for Invasion and Saturation by Emerging Pathogens and Pests

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