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Common themes in nutrient acquisition by plant symbiotic microbes, described by the Gene Ontology.

Chibucos MC, Tyler BM - BMC Microbiol. (2009)

Bottom Line: Relationships between hosts and symbionts range from biotrophic mutualism to necrotrophic parasitism, with a corresponding range of structures to facilitate nutrient flow between host and symbiont.We show how Gene Ontology (GO) terms developed by the Plant-Associated Microbe Gene Ontology (PAMGO) Consortium can be used for describing commonalities in nutrient acquisition among diverse plant symbionts.Where appropriate, parallels found among animal symbionts are also highlighted.

View Article: PubMed Central - HTML - PubMed

Affiliation: Virginia Bioinformatics Institute, Virginia Polytechnic Institute and State University, Blacksburg, VA 24061, USA. mchibucos@som.umaryland.edu

ABSTRACT
A critical function for symbionts is the acquisition of nutrients from their host. Relationships between hosts and symbionts range from biotrophic mutualism to necrotrophic parasitism, with a corresponding range of structures to facilitate nutrient flow between host and symbiont. Here, we review common themes among the nutrient acquisition strategies of a range of plant symbiotic microorganisms, including mutualistic symbionts, biotrophic pathogens that feed from living tissue, necrotrophic pathogens that kill host tissue, and hemibiotrophic pathogens that switch from biotrophy to necrotrophy. We show how Gene Ontology (GO) terms developed by the Plant-Associated Microbe Gene Ontology (PAMGO) Consortium can be used for describing commonalities in nutrient acquisition among diverse plant symbionts. Where appropriate, parallels found among animal symbionts are also highlighted.

Show MeSH
Gene Ontology terms relevant to three phases of symbiotic nutrient exchange. Processes associated with phases I and II of nutrient exchange are described by GO terms from the "GO: 0008150 biological_process" ontology. Terms at the top of the diagram describe higher level processes, terms in the middle represent symbiont processes, and terms at the bottom characterize host processes. Functions associated with phase III are described with GO terms from the "GO: 0003674 molecular_function" ontology that describe nutrient uptake irrespective of symbiotic partner. In the GO, term relationships take the form of a directed acyclic graph (DAG), similar to a hierarchy, except that a given term can have multiple parent terms or multiple child terms. Here, for simplicity, only selected terms are shown, and only a subset of the parent-child relationships are depicted; arrows symbolize GO "is_a" and "part_of" relationships (for more information on term relationships and other aspects ontology structure, i.e. "is_a", "part_of", and "regulates," see [9]). Some dashed arrows are used to enhance readability. GO terms highlighted by dark ovals represent GO terms also shown in Figure 1, and terms filled with grey can be found in the text.
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Figure 2: Gene Ontology terms relevant to three phases of symbiotic nutrient exchange. Processes associated with phases I and II of nutrient exchange are described by GO terms from the "GO: 0008150 biological_process" ontology. Terms at the top of the diagram describe higher level processes, terms in the middle represent symbiont processes, and terms at the bottom characterize host processes. Functions associated with phase III are described with GO terms from the "GO: 0003674 molecular_function" ontology that describe nutrient uptake irrespective of symbiotic partner. In the GO, term relationships take the form of a directed acyclic graph (DAG), similar to a hierarchy, except that a given term can have multiple parent terms or multiple child terms. Here, for simplicity, only selected terms are shown, and only a subset of the parent-child relationships are depicted; arrows symbolize GO "is_a" and "part_of" relationships (for more information on term relationships and other aspects ontology structure, i.e. "is_a", "part_of", and "regulates," see [9]). Some dashed arrows are used to enhance readability. GO terms highlighted by dark ovals represent GO terms also shown in Figure 1, and terms filled with grey can be found in the text.

Mentions: In the GO, the concept of symbiosis is represented by the term "GO: 0044403 symbiosis, encompassing mutualism through parasitism", which is defined as: "An interaction between two organisms living together in more or less intimate association. The term host is usually used for the larger (macro) of the two members of a symbiosis. The smaller (micro) member is called the symbiont organism" [10]. The various forms of symbiosis include parasitism, in which the association is disadvantageous or destructive to the host organism; mutualism, in which the association is advantageous to both; and commensalism, in which the symbiont benefits while the host is not affected [8]. However, mutualism, parasitism, and commensalism are not discrete categories of interactions but rather a continuum. In fact, the nature of a symbiotic interaction may vary due to developmental changes in the host or symbiont, changes in the biotic or abiotic environment, or variation in host genotype [11]. Correspondingly, the exchange of nutrients between symbiotic partners may be context dependent and may be bidirectional or heavily unidirectional. The PAMGO Consortium strongly discourages the common but incorrect usage of the term "symbiosis" as a synonym for "mutualism" [8]. Figure 1 illustrates parent and child terms of "GO: 0044403 symbiosis, encompassing mutualism through parasitism", as viewed with the AmiGO browser [10]. Examples of child terms describing biological processes related directly or peripherally to nutritional exchange between symbionts and hosts include: "GO: 00051816 acquisition of nutrients from other organism during symbiotic interaction"; "GO: 0051817 modification of morphology or physiology of other organism during symbiotic interaction"; and "GO: 0009877 nodulation". These and other terms are described in greater detail in Figure 2 and Additional file 1.


Common themes in nutrient acquisition by plant symbiotic microbes, described by the Gene Ontology.

Chibucos MC, Tyler BM - BMC Microbiol. (2009)

Gene Ontology terms relevant to three phases of symbiotic nutrient exchange. Processes associated with phases I and II of nutrient exchange are described by GO terms from the "GO: 0008150 biological_process" ontology. Terms at the top of the diagram describe higher level processes, terms in the middle represent symbiont processes, and terms at the bottom characterize host processes. Functions associated with phase III are described with GO terms from the "GO: 0003674 molecular_function" ontology that describe nutrient uptake irrespective of symbiotic partner. In the GO, term relationships take the form of a directed acyclic graph (DAG), similar to a hierarchy, except that a given term can have multiple parent terms or multiple child terms. Here, for simplicity, only selected terms are shown, and only a subset of the parent-child relationships are depicted; arrows symbolize GO "is_a" and "part_of" relationships (for more information on term relationships and other aspects ontology structure, i.e. "is_a", "part_of", and "regulates," see [9]). Some dashed arrows are used to enhance readability. GO terms highlighted by dark ovals represent GO terms also shown in Figure 1, and terms filled with grey can be found in the text.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2654666&req=5

Figure 2: Gene Ontology terms relevant to three phases of symbiotic nutrient exchange. Processes associated with phases I and II of nutrient exchange are described by GO terms from the "GO: 0008150 biological_process" ontology. Terms at the top of the diagram describe higher level processes, terms in the middle represent symbiont processes, and terms at the bottom characterize host processes. Functions associated with phase III are described with GO terms from the "GO: 0003674 molecular_function" ontology that describe nutrient uptake irrespective of symbiotic partner. In the GO, term relationships take the form of a directed acyclic graph (DAG), similar to a hierarchy, except that a given term can have multiple parent terms or multiple child terms. Here, for simplicity, only selected terms are shown, and only a subset of the parent-child relationships are depicted; arrows symbolize GO "is_a" and "part_of" relationships (for more information on term relationships and other aspects ontology structure, i.e. "is_a", "part_of", and "regulates," see [9]). Some dashed arrows are used to enhance readability. GO terms highlighted by dark ovals represent GO terms also shown in Figure 1, and terms filled with grey can be found in the text.
Mentions: In the GO, the concept of symbiosis is represented by the term "GO: 0044403 symbiosis, encompassing mutualism through parasitism", which is defined as: "An interaction between two organisms living together in more or less intimate association. The term host is usually used for the larger (macro) of the two members of a symbiosis. The smaller (micro) member is called the symbiont organism" [10]. The various forms of symbiosis include parasitism, in which the association is disadvantageous or destructive to the host organism; mutualism, in which the association is advantageous to both; and commensalism, in which the symbiont benefits while the host is not affected [8]. However, mutualism, parasitism, and commensalism are not discrete categories of interactions but rather a continuum. In fact, the nature of a symbiotic interaction may vary due to developmental changes in the host or symbiont, changes in the biotic or abiotic environment, or variation in host genotype [11]. Correspondingly, the exchange of nutrients between symbiotic partners may be context dependent and may be bidirectional or heavily unidirectional. The PAMGO Consortium strongly discourages the common but incorrect usage of the term "symbiosis" as a synonym for "mutualism" [8]. Figure 1 illustrates parent and child terms of "GO: 0044403 symbiosis, encompassing mutualism through parasitism", as viewed with the AmiGO browser [10]. Examples of child terms describing biological processes related directly or peripherally to nutritional exchange between symbionts and hosts include: "GO: 00051816 acquisition of nutrients from other organism during symbiotic interaction"; "GO: 0051817 modification of morphology or physiology of other organism during symbiotic interaction"; and "GO: 0009877 nodulation". These and other terms are described in greater detail in Figure 2 and Additional file 1.

Bottom Line: Relationships between hosts and symbionts range from biotrophic mutualism to necrotrophic parasitism, with a corresponding range of structures to facilitate nutrient flow between host and symbiont.We show how Gene Ontology (GO) terms developed by the Plant-Associated Microbe Gene Ontology (PAMGO) Consortium can be used for describing commonalities in nutrient acquisition among diverse plant symbionts.Where appropriate, parallels found among animal symbionts are also highlighted.

View Article: PubMed Central - HTML - PubMed

Affiliation: Virginia Bioinformatics Institute, Virginia Polytechnic Institute and State University, Blacksburg, VA 24061, USA. mchibucos@som.umaryland.edu

ABSTRACT
A critical function for symbionts is the acquisition of nutrients from their host. Relationships between hosts and symbionts range from biotrophic mutualism to necrotrophic parasitism, with a corresponding range of structures to facilitate nutrient flow between host and symbiont. Here, we review common themes among the nutrient acquisition strategies of a range of plant symbiotic microorganisms, including mutualistic symbionts, biotrophic pathogens that feed from living tissue, necrotrophic pathogens that kill host tissue, and hemibiotrophic pathogens that switch from biotrophy to necrotrophy. We show how Gene Ontology (GO) terms developed by the Plant-Associated Microbe Gene Ontology (PAMGO) Consortium can be used for describing commonalities in nutrient acquisition among diverse plant symbionts. Where appropriate, parallels found among animal symbionts are also highlighted.

Show MeSH