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Plant and pathogen nutrient acquisition strategies.

Fatima U, Senthil-Kumar M - Front Plant Sci (2015)

Bottom Line: In addition, we highlight the current status of our understanding about the nutrient acquisition strategies used by bacterial pathogens, namely targeting the sugar transporters that are dedicated for the plant's growth and development.Bacterial strategies for altering the plant cell membrane permeability to enhance the release of nutrients are also enumerated along with in-depth analysis of molecular mechanisms behind these strategies.The information presented in this review will be useful to understand the plant-pathogen interaction in nutrient perspective.

View Article: PubMed Central - PubMed

Affiliation: National Institute of Plant Genome Research New Delhi, India.

ABSTRACT
Nutrients are indispensable elements required for the growth of all living organisms including plants and pathogens. Phyllosphere, rhizosphere, apoplast, phloem, xylem, and cell organelles are the nutrient niches in plants that are the target of bacterial pathogens. Depending upon nutrients availability, the pathogen adapts various acquisition strategies and inhabits the specific niche. In this review, we discuss the nutrient composition of different niches in plants, the mechanisms involved in the recognition of nutrient niche and the sophisticated strategies used by the bacterial pathogens for acquiring nutrients. We provide insight into various nutrient acquisition strategies used by necrotrophic, biotrophic, and hemibiotrophic bacteria. Specifically we discuss both modulation of bacterial machinery and manipulation of host machinery. In addition, we highlight the current status of our understanding about the nutrient acquisition strategies used by bacterial pathogens, namely targeting the sugar transporters that are dedicated for the plant's growth and development. Bacterial strategies for altering the plant cell membrane permeability to enhance the release of nutrients are also enumerated along with in-depth analysis of molecular mechanisms behind these strategies. The information presented in this review will be useful to understand the plant-pathogen interaction in nutrient perspective.

No MeSH data available.


Overview of molecular and biochemical events used by biotrophic or hemibiotrophic bacteria to acquire nutrients during apoplast colonization. Pathogenic bacteria use several strategies to acquire nutrients. They can either modulate their own machinery or manipulate plant cell machinery to acquire nutrients. During modulation of their own machinery, bacteria activate various transporters and take up nutrients that are present in apoplast. They can secrete cellulose degrading enzyme to release cell wall-bound nutrients (Cw-Inv). For uptake of less preferred nutrients they use two different ways. First, by secreting enzyme in apoplasm that converts undesirable form of nutrient into desirable form and then take up that desirable form of nutrient by transporter. Second, the uptake of less preferred nutrient by specific transporter and then suitably metabolize its energy. Sucrose specific phosphotransferase system is shown here for uptake of sucrose in the form of sucrose-6-phosphate (S6P) and catabolize it into fructose (F) and glucose-6-phosphate (G6P). Type III secretion system (TTSS) delivered effectors target expression of sugar transporter-encoding genes of host cell. Effector-mediated induction of SWEET (sugar will eventually be exported transporter) transporter for increasing sugar efflux in apoplast is shown here. Also induction of sugar biosynthesis genes for high sugar synthesis in cytosol and its movement to apoplast is shown. Expression of host cell wall-invertase-mediated conversion of sucrose into glucose and fructose in apoplast is depicted. α-Ketoglutaric acid transporter (KgtP) secreted by bacterial pathogen though TTSS and its localization in host cell membrane and the efflux of α-ketoglutaric acid from host cell into apoplasm is illustrated. Enzyme II BC, Fructose specific phosphotransferase system; SSPTS, Sucrose-specific phosphotransferase system; gltK, glucose ATP-binding cassette transporters (ABC) transporter permease; mgtE, magnesium transporter; fecC, Iron ABC transporter permease; sulP, sulphatepermease; piT, inorganic phosphate transporter; gltP, proton/glutamate symport; gabP, gamma-amino butyric acid (GABA) permease; madM, malonate transporter; citH, citrate/proton symport; dctA1, dicarboxylate transporter; kgtP, ketoglutaric acid transporter; egl, endoglucanase; cbhA, cellobiohydrolase; f6p, fructose-6-phosphate. Black arrow indicates influx or efflux of nutrients. Red arrow indicates extracellular enzyme secretion. Violet arrow indicates extracellular enzymatic reaction. Blue arrow indicates entry of nutrient into metabolic pathway. Green arrow indicates delivery through TTSS. Cylinder indicates transporter. Plus sign indicates induction of genes.
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Figure 2: Overview of molecular and biochemical events used by biotrophic or hemibiotrophic bacteria to acquire nutrients during apoplast colonization. Pathogenic bacteria use several strategies to acquire nutrients. They can either modulate their own machinery or manipulate plant cell machinery to acquire nutrients. During modulation of their own machinery, bacteria activate various transporters and take up nutrients that are present in apoplast. They can secrete cellulose degrading enzyme to release cell wall-bound nutrients (Cw-Inv). For uptake of less preferred nutrients they use two different ways. First, by secreting enzyme in apoplasm that converts undesirable form of nutrient into desirable form and then take up that desirable form of nutrient by transporter. Second, the uptake of less preferred nutrient by specific transporter and then suitably metabolize its energy. Sucrose specific phosphotransferase system is shown here for uptake of sucrose in the form of sucrose-6-phosphate (S6P) and catabolize it into fructose (F) and glucose-6-phosphate (G6P). Type III secretion system (TTSS) delivered effectors target expression of sugar transporter-encoding genes of host cell. Effector-mediated induction of SWEET (sugar will eventually be exported transporter) transporter for increasing sugar efflux in apoplast is shown here. Also induction of sugar biosynthesis genes for high sugar synthesis in cytosol and its movement to apoplast is shown. Expression of host cell wall-invertase-mediated conversion of sucrose into glucose and fructose in apoplast is depicted. α-Ketoglutaric acid transporter (KgtP) secreted by bacterial pathogen though TTSS and its localization in host cell membrane and the efflux of α-ketoglutaric acid from host cell into apoplasm is illustrated. Enzyme II BC, Fructose specific phosphotransferase system; SSPTS, Sucrose-specific phosphotransferase system; gltK, glucose ATP-binding cassette transporters (ABC) transporter permease; mgtE, magnesium transporter; fecC, Iron ABC transporter permease; sulP, sulphatepermease; piT, inorganic phosphate transporter; gltP, proton/glutamate symport; gabP, gamma-amino butyric acid (GABA) permease; madM, malonate transporter; citH, citrate/proton symport; dctA1, dicarboxylate transporter; kgtP, ketoglutaric acid transporter; egl, endoglucanase; cbhA, cellobiohydrolase; f6p, fructose-6-phosphate. Black arrow indicates influx or efflux of nutrients. Red arrow indicates extracellular enzyme secretion. Violet arrow indicates extracellular enzymatic reaction. Blue arrow indicates entry of nutrient into metabolic pathway. Green arrow indicates delivery through TTSS. Cylinder indicates transporter. Plus sign indicates induction of genes.

Mentions: The first strategy for obtaining nutrients from niches involves the use of transporters present in the pathogen. Porins present in bacterial membrane allow the passive diffusion of nutrients available in plant niches. These pore-forming proteins are abundant in several species of Pseudomonas (Delmotte et al., 2009). Bacterial pathogens also use different types of transporters for the active uptake of nutrients (Figure 2). ATP-binding cassette transporters (ABC-transporters) and TonB-dependent transporters (TBDTs) are the important transporters involved in nutrient uptake (Delmotte et al., 2009). For example, ABC-transporters present in Pseudomonas species facilitate the uptake of maltose, glucose and sucrose as well as amino acids and minerals (Delmotte et al., 2009). TBDTs are known to be involved in iron or vitamin B12 uptake. These transporters are also shown to facilitate the uptake of carbohydrates present in low amounts on the leaf surfaces (Lindow and Brandl, 2003; Vorholt, 2012). Genomes of several species of Xanthomonas, Sphingomonas, and Pseudomonas are known to have high representation of TBDT genes. For example, the genomes of X. campestris pv. campestris (causal agent of black rot of crucifers), P. syringae pv. tomato DC3000 and P. syringae pv. syringae (causal agent of blight of barely) have 72, 25, and 19 TBDT genes, respectively (Blanvillain et al., 2007; Cornelis and Bodilis, 2009). During phyllosphere colonization, X. campestris pv. campestris encounters nutrient limited environment on the leaf surfaces. Under these conditions, TBDT has been shown to transport sucrose available in the phyllosphere (Blanvillain et al., 2007). Similarly, the genome of X. albilineans (causal agent of sugarcane leaf scald) has 35 putative TBDT genes. During their xylem colonization, TBDT is involved in the transport of plant cell wall derived nutrients like maltose, xylan, xylose, pectin, polygalacturonate, and arabinose (Blanvillain et al., 2007; Pieretti et al., 2012; De Bernonville et al., 2014). These studies show that bacterial pathogens are adapted to live in nutrient-poor environments by scavenging the plant carbohydrates through TBDTs. Other studies indicate that bacterial pathogens preferentially utilize some carbon sources over others. Therefore, they highly express genes encoding transporters that specifically facilitate the uptake of preferred carbon sources present in the niche. For example, some species of Pseudomonas and Xanthomonas preferentially utilize dicarboxylates such as malate, citrate and succinate over other carbon sources present in the apoplast. Dicarboxylate transporter (DctA1) of P. syringae pv. tomato strain facilitates the uptake of TCA cycle intermediates (Mellgren et al., 2009). Similarly, citrate transporter (CitH) of X. campestris pv. vesicatoria facilitates the citrate uptake and it is important for this bacterial virulence in tomato plants (Tamir-Ariel et al., 2011).


Plant and pathogen nutrient acquisition strategies.

Fatima U, Senthil-Kumar M - Front Plant Sci (2015)

Overview of molecular and biochemical events used by biotrophic or hemibiotrophic bacteria to acquire nutrients during apoplast colonization. Pathogenic bacteria use several strategies to acquire nutrients. They can either modulate their own machinery or manipulate plant cell machinery to acquire nutrients. During modulation of their own machinery, bacteria activate various transporters and take up nutrients that are present in apoplast. They can secrete cellulose degrading enzyme to release cell wall-bound nutrients (Cw-Inv). For uptake of less preferred nutrients they use two different ways. First, by secreting enzyme in apoplasm that converts undesirable form of nutrient into desirable form and then take up that desirable form of nutrient by transporter. Second, the uptake of less preferred nutrient by specific transporter and then suitably metabolize its energy. Sucrose specific phosphotransferase system is shown here for uptake of sucrose in the form of sucrose-6-phosphate (S6P) and catabolize it into fructose (F) and glucose-6-phosphate (G6P). Type III secretion system (TTSS) delivered effectors target expression of sugar transporter-encoding genes of host cell. Effector-mediated induction of SWEET (sugar will eventually be exported transporter) transporter for increasing sugar efflux in apoplast is shown here. Also induction of sugar biosynthesis genes for high sugar synthesis in cytosol and its movement to apoplast is shown. Expression of host cell wall-invertase-mediated conversion of sucrose into glucose and fructose in apoplast is depicted. α-Ketoglutaric acid transporter (KgtP) secreted by bacterial pathogen though TTSS and its localization in host cell membrane and the efflux of α-ketoglutaric acid from host cell into apoplasm is illustrated. Enzyme II BC, Fructose specific phosphotransferase system; SSPTS, Sucrose-specific phosphotransferase system; gltK, glucose ATP-binding cassette transporters (ABC) transporter permease; mgtE, magnesium transporter; fecC, Iron ABC transporter permease; sulP, sulphatepermease; piT, inorganic phosphate transporter; gltP, proton/glutamate symport; gabP, gamma-amino butyric acid (GABA) permease; madM, malonate transporter; citH, citrate/proton symport; dctA1, dicarboxylate transporter; kgtP, ketoglutaric acid transporter; egl, endoglucanase; cbhA, cellobiohydrolase; f6p, fructose-6-phosphate. Black arrow indicates influx or efflux of nutrients. Red arrow indicates extracellular enzyme secretion. Violet arrow indicates extracellular enzymatic reaction. Blue arrow indicates entry of nutrient into metabolic pathway. Green arrow indicates delivery through TTSS. Cylinder indicates transporter. Plus sign indicates induction of genes.
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Figure 2: Overview of molecular and biochemical events used by biotrophic or hemibiotrophic bacteria to acquire nutrients during apoplast colonization. Pathogenic bacteria use several strategies to acquire nutrients. They can either modulate their own machinery or manipulate plant cell machinery to acquire nutrients. During modulation of their own machinery, bacteria activate various transporters and take up nutrients that are present in apoplast. They can secrete cellulose degrading enzyme to release cell wall-bound nutrients (Cw-Inv). For uptake of less preferred nutrients they use two different ways. First, by secreting enzyme in apoplasm that converts undesirable form of nutrient into desirable form and then take up that desirable form of nutrient by transporter. Second, the uptake of less preferred nutrient by specific transporter and then suitably metabolize its energy. Sucrose specific phosphotransferase system is shown here for uptake of sucrose in the form of sucrose-6-phosphate (S6P) and catabolize it into fructose (F) and glucose-6-phosphate (G6P). Type III secretion system (TTSS) delivered effectors target expression of sugar transporter-encoding genes of host cell. Effector-mediated induction of SWEET (sugar will eventually be exported transporter) transporter for increasing sugar efflux in apoplast is shown here. Also induction of sugar biosynthesis genes for high sugar synthesis in cytosol and its movement to apoplast is shown. Expression of host cell wall-invertase-mediated conversion of sucrose into glucose and fructose in apoplast is depicted. α-Ketoglutaric acid transporter (KgtP) secreted by bacterial pathogen though TTSS and its localization in host cell membrane and the efflux of α-ketoglutaric acid from host cell into apoplasm is illustrated. Enzyme II BC, Fructose specific phosphotransferase system; SSPTS, Sucrose-specific phosphotransferase system; gltK, glucose ATP-binding cassette transporters (ABC) transporter permease; mgtE, magnesium transporter; fecC, Iron ABC transporter permease; sulP, sulphatepermease; piT, inorganic phosphate transporter; gltP, proton/glutamate symport; gabP, gamma-amino butyric acid (GABA) permease; madM, malonate transporter; citH, citrate/proton symport; dctA1, dicarboxylate transporter; kgtP, ketoglutaric acid transporter; egl, endoglucanase; cbhA, cellobiohydrolase; f6p, fructose-6-phosphate. Black arrow indicates influx or efflux of nutrients. Red arrow indicates extracellular enzyme secretion. Violet arrow indicates extracellular enzymatic reaction. Blue arrow indicates entry of nutrient into metabolic pathway. Green arrow indicates delivery through TTSS. Cylinder indicates transporter. Plus sign indicates induction of genes.
Mentions: The first strategy for obtaining nutrients from niches involves the use of transporters present in the pathogen. Porins present in bacterial membrane allow the passive diffusion of nutrients available in plant niches. These pore-forming proteins are abundant in several species of Pseudomonas (Delmotte et al., 2009). Bacterial pathogens also use different types of transporters for the active uptake of nutrients (Figure 2). ATP-binding cassette transporters (ABC-transporters) and TonB-dependent transporters (TBDTs) are the important transporters involved in nutrient uptake (Delmotte et al., 2009). For example, ABC-transporters present in Pseudomonas species facilitate the uptake of maltose, glucose and sucrose as well as amino acids and minerals (Delmotte et al., 2009). TBDTs are known to be involved in iron or vitamin B12 uptake. These transporters are also shown to facilitate the uptake of carbohydrates present in low amounts on the leaf surfaces (Lindow and Brandl, 2003; Vorholt, 2012). Genomes of several species of Xanthomonas, Sphingomonas, and Pseudomonas are known to have high representation of TBDT genes. For example, the genomes of X. campestris pv. campestris (causal agent of black rot of crucifers), P. syringae pv. tomato DC3000 and P. syringae pv. syringae (causal agent of blight of barely) have 72, 25, and 19 TBDT genes, respectively (Blanvillain et al., 2007; Cornelis and Bodilis, 2009). During phyllosphere colonization, X. campestris pv. campestris encounters nutrient limited environment on the leaf surfaces. Under these conditions, TBDT has been shown to transport sucrose available in the phyllosphere (Blanvillain et al., 2007). Similarly, the genome of X. albilineans (causal agent of sugarcane leaf scald) has 35 putative TBDT genes. During their xylem colonization, TBDT is involved in the transport of plant cell wall derived nutrients like maltose, xylan, xylose, pectin, polygalacturonate, and arabinose (Blanvillain et al., 2007; Pieretti et al., 2012; De Bernonville et al., 2014). These studies show that bacterial pathogens are adapted to live in nutrient-poor environments by scavenging the plant carbohydrates through TBDTs. Other studies indicate that bacterial pathogens preferentially utilize some carbon sources over others. Therefore, they highly express genes encoding transporters that specifically facilitate the uptake of preferred carbon sources present in the niche. For example, some species of Pseudomonas and Xanthomonas preferentially utilize dicarboxylates such as malate, citrate and succinate over other carbon sources present in the apoplast. Dicarboxylate transporter (DctA1) of P. syringae pv. tomato strain facilitates the uptake of TCA cycle intermediates (Mellgren et al., 2009). Similarly, citrate transporter (CitH) of X. campestris pv. vesicatoria facilitates the citrate uptake and it is important for this bacterial virulence in tomato plants (Tamir-Ariel et al., 2011).

Bottom Line: In addition, we highlight the current status of our understanding about the nutrient acquisition strategies used by bacterial pathogens, namely targeting the sugar transporters that are dedicated for the plant's growth and development.Bacterial strategies for altering the plant cell membrane permeability to enhance the release of nutrients are also enumerated along with in-depth analysis of molecular mechanisms behind these strategies.The information presented in this review will be useful to understand the plant-pathogen interaction in nutrient perspective.

View Article: PubMed Central - PubMed

Affiliation: National Institute of Plant Genome Research New Delhi, India.

ABSTRACT
Nutrients are indispensable elements required for the growth of all living organisms including plants and pathogens. Phyllosphere, rhizosphere, apoplast, phloem, xylem, and cell organelles are the nutrient niches in plants that are the target of bacterial pathogens. Depending upon nutrients availability, the pathogen adapts various acquisition strategies and inhabits the specific niche. In this review, we discuss the nutrient composition of different niches in plants, the mechanisms involved in the recognition of nutrient niche and the sophisticated strategies used by the bacterial pathogens for acquiring nutrients. We provide insight into various nutrient acquisition strategies used by necrotrophic, biotrophic, and hemibiotrophic bacteria. Specifically we discuss both modulation of bacterial machinery and manipulation of host machinery. In addition, we highlight the current status of our understanding about the nutrient acquisition strategies used by bacterial pathogens, namely targeting the sugar transporters that are dedicated for the plant's growth and development. Bacterial strategies for altering the plant cell membrane permeability to enhance the release of nutrients are also enumerated along with in-depth analysis of molecular mechanisms behind these strategies. The information presented in this review will be useful to understand the plant-pathogen interaction in nutrient perspective.

No MeSH data available.