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A proposed mechanism for nitrogen acquisition by grass seedlings through oxidation of symbiotic bacteria.

White JF, Crawford H, Torres MS, Mattera R, Irizarry I, Bergen M - Symbiosis (2012)

Bottom Line: Experiments on this proposed mechanism employ tall fescue (Festuca arundinaceae) seedlings to elucidate features of the oxidative mechanism.We also made surveys of the seedlings of several grass species to assess the distribution of the phenomenon of microbial oxidation in the Poaceae.Hydrogen peroxide secretion from seedling roots and bacterial oxidation was observed in several species in subfamily Pooideae where seeds possessed adherent paleas and lemmas, but was not seen in grasses that lacked this feature or long-cultivated crop species.

View Article: PubMed Central - PubMed

Affiliation: Department of Plant Biology and Pathology, Rutgers University, New Brunswick, NJ USA.

ABSTRACT
In this paper we propose and provide evidence for a mechanism, oxidative nitrogen scavenging (ONS), whereby seedlings of some grass species may extract nitrogen from symbiotic diazotrophic bacteria through oxidation by plant-secreted reactive oxygen species (ROS). Experiments on this proposed mechanism employ tall fescue (Festuca arundinaceae) seedlings to elucidate features of the oxidative mechanism. We employed 15N(2) gas assimilation experiments to demonstrate nitrogen fixation, direct microscopic visualization of bacteria on seedling surfaces to visualize the bacterial oxidation process, reactive oxygen probes to test for the presence of H(2)O(2) and cultural experiments to assess conditions under which H(2)O(2) is secreted by seedlings. We also made surveys of the seedlings of several grass species to assess the distribution of the phenomenon of microbial oxidation in the Poaceae. Key elements of the proposed mechanism for nitrogen acquisition in seedlings include: 1) diazotrophic bacteria are vectored on or within seeds; 2) at seed germination bacteria colonize seedling roots and shoots; 3) seedling tissues secrete ROS onto bacteria; 4) bacterial cell walls, membranes, nucleic acids, proteins and other biological molecules are oxidized; 5) nitrates and/or smaller fragments of organic nitrogen-containing molecules resulting from oxidation may be absorbed by seedling tissues and larger peptide fragments may be further processed by secreted or cell wall plant proteases until they are small enough for transport into cells. Hydrogen peroxide secretion from seedling roots and bacterial oxidation was observed in several species in subfamily Pooideae where seeds possessed adherent paleas and lemmas, but was not seen in grasses that lacked this feature or long-cultivated crop species.

No MeSH data available.


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a–d. Root tissues and bacteria stained with SYTO9 florescent nucleic acid stain. a and b Root hairs showing epiphytic swollen oxidizing bacteria (arrows) with intact bacteria in background; c Root parenchyma showing intensely staining intact bacteria (yellow arrows) and masses of oxidizing bacteria (blue arrow); d Root parenchyma showing nucleic acid rings (bulls-eye rings) around oxidizing bacteria (arrows)
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Fig2: a–d. Root tissues and bacteria stained with SYTO9 florescent nucleic acid stain. a and b Root hairs showing epiphytic swollen oxidizing bacteria (arrows) with intact bacteria in background; c Root parenchyma showing intensely staining intact bacteria (yellow arrows) and masses of oxidizing bacteria (blue arrow); d Root parenchyma showing nucleic acid rings (bulls-eye rings) around oxidizing bacteria (arrows)

Mentions: To visualize bacterial oxidation on seedlings, we stained plates bearing seedlings with DAB/horseradish peroxidase for a 10 h period. We then excised seedling roots and shoots, placed them on a slide containing 1 % aniline blue/lactic acid stain, and examined the slide using bright field microscopy (Bacon and White 1994). On a second set of slides, we stained seedling roots (to visualize nucleic acids during oxidation) with SYTO9® (Life Technologies, Carlsbad, CA) and observed them using fluorescence microscopy on a Zeiss Axioskop (using the FITC filter system (range 430–520 nm for Fig. 2a and b; and blue violet excitation (range 395–440 nm) for Fig. 2c and d).


A proposed mechanism for nitrogen acquisition by grass seedlings through oxidation of symbiotic bacteria.

White JF, Crawford H, Torres MS, Mattera R, Irizarry I, Bergen M - Symbiosis (2012)

a–d. Root tissues and bacteria stained with SYTO9 florescent nucleic acid stain. a and b Root hairs showing epiphytic swollen oxidizing bacteria (arrows) with intact bacteria in background; c Root parenchyma showing intensely staining intact bacteria (yellow arrows) and masses of oxidizing bacteria (blue arrow); d Root parenchyma showing nucleic acid rings (bulls-eye rings) around oxidizing bacteria (arrows)
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3473182&req=5

Fig2: a–d. Root tissues and bacteria stained with SYTO9 florescent nucleic acid stain. a and b Root hairs showing epiphytic swollen oxidizing bacteria (arrows) with intact bacteria in background; c Root parenchyma showing intensely staining intact bacteria (yellow arrows) and masses of oxidizing bacteria (blue arrow); d Root parenchyma showing nucleic acid rings (bulls-eye rings) around oxidizing bacteria (arrows)
Mentions: To visualize bacterial oxidation on seedlings, we stained plates bearing seedlings with DAB/horseradish peroxidase for a 10 h period. We then excised seedling roots and shoots, placed them on a slide containing 1 % aniline blue/lactic acid stain, and examined the slide using bright field microscopy (Bacon and White 1994). On a second set of slides, we stained seedling roots (to visualize nucleic acids during oxidation) with SYTO9® (Life Technologies, Carlsbad, CA) and observed them using fluorescence microscopy on a Zeiss Axioskop (using the FITC filter system (range 430–520 nm for Fig. 2a and b; and blue violet excitation (range 395–440 nm) for Fig. 2c and d).

Bottom Line: Experiments on this proposed mechanism employ tall fescue (Festuca arundinaceae) seedlings to elucidate features of the oxidative mechanism.We also made surveys of the seedlings of several grass species to assess the distribution of the phenomenon of microbial oxidation in the Poaceae.Hydrogen peroxide secretion from seedling roots and bacterial oxidation was observed in several species in subfamily Pooideae where seeds possessed adherent paleas and lemmas, but was not seen in grasses that lacked this feature or long-cultivated crop species.

View Article: PubMed Central - PubMed

Affiliation: Department of Plant Biology and Pathology, Rutgers University, New Brunswick, NJ USA.

ABSTRACT
In this paper we propose and provide evidence for a mechanism, oxidative nitrogen scavenging (ONS), whereby seedlings of some grass species may extract nitrogen from symbiotic diazotrophic bacteria through oxidation by plant-secreted reactive oxygen species (ROS). Experiments on this proposed mechanism employ tall fescue (Festuca arundinaceae) seedlings to elucidate features of the oxidative mechanism. We employed 15N(2) gas assimilation experiments to demonstrate nitrogen fixation, direct microscopic visualization of bacteria on seedling surfaces to visualize the bacterial oxidation process, reactive oxygen probes to test for the presence of H(2)O(2) and cultural experiments to assess conditions under which H(2)O(2) is secreted by seedlings. We also made surveys of the seedlings of several grass species to assess the distribution of the phenomenon of microbial oxidation in the Poaceae. Key elements of the proposed mechanism for nitrogen acquisition in seedlings include: 1) diazotrophic bacteria are vectored on or within seeds; 2) at seed germination bacteria colonize seedling roots and shoots; 3) seedling tissues secrete ROS onto bacteria; 4) bacterial cell walls, membranes, nucleic acids, proteins and other biological molecules are oxidized; 5) nitrates and/or smaller fragments of organic nitrogen-containing molecules resulting from oxidation may be absorbed by seedling tissues and larger peptide fragments may be further processed by secreted or cell wall plant proteases until they are small enough for transport into cells. Hydrogen peroxide secretion from seedling roots and bacterial oxidation was observed in several species in subfamily Pooideae where seeds possessed adherent paleas and lemmas, but was not seen in grasses that lacked this feature or long-cultivated crop species.

No MeSH data available.


Related in: MedlinePlus