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Article

Histochemical Evidence for Nitrogen-Transfer Endosymbiosis in Non-Photosynthetic Cells of Leaves and Inflorescence Bracts of Angiosperms

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Department of Plant Biology, Rutgers University, New Brunswick, NJ 08901, USA
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Department of Biochemistry and Microbiology, Rutgers University, New Brunswick, NJ 08901, USA
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School of Health and Sciences, Universidad del Sagrado Corazón, San Juan 00914, Puerto Rico
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US Geological Survey Great Lakes Science Center, Ann Arbor, MI 48105, USA
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Max Planck Tandem Group in Plant Microbial Ecology, Universidad del Valle, Cali 760043, Colombia
*
Authors to whom correspondence should be addressed.
Academic Editors: Christian Staehelin and Bernard R. Glick
Biology 2022, 11(6), 876; https://doi.org/10.3390/biology11060876
Received: 25 March 2022 / Revised: 15 May 2022 / Accepted: 1 June 2022 / Published: 7 June 2022
We used light and confocal microscopy to visualize bacteria in leaf and bract cells of more than 30 species in 18 families of seed plants. We detected chemical exchanges between intracellular bacteria and plant cells. We found that endophytic bacteria that show evidence of the transfer of nitrogen to plants are present in non-photosynthetic cells of leaves and bracts of diverse plant species. Nitrogen transfer from bacteria was observed in epidermal cells, various filamentous and glandular trichomes, and other non-photosynthetic cells. The most efficient of the nitrogen-transfer endosymbioses were seen to involve glandular trichomes, as seen in hops (Humulus lupulus) and hemp (Cannabis sativa). Trichome chemistry is hypothesized to function to scavenge oxygen around bacteria to facilitate nitrogen fixation.
We used light and confocal microscopy to visualize bacteria in leaf and bract cells of more than 30 species in 18 families of seed plants. Through histochemical analysis, we detected hormones (including ethylene and nitric oxide), superoxide, and nitrogenous chemicals (including nitric oxide and nitrate) around bacteria within plant cells. Bacteria were observed in epidermal cells, various filamentous and glandular trichomes, and other non-photosynthetic cells. Most notably, bacteria showing nitrate formation based on histochemical staining were present in glandular trichomes of some dicots (e.g., Humulus lupulus and Cannabis sativa). Glandular trichome chemistry is hypothesized to function to scavenge oxygen around bacteria and reduce oxidative damage to intracellular bacterial cells. Experiments to assess the differential absorption of isotopic nitrogen into plants suggest the assimilation of nitrogen into actively growing tissues of plants, where bacteria are most active and carbohydrates are more available. The leaf and bract cell endosymbiosis types outlined in this paper have not been previously reported and may be important in facilitating plant growth, development, oxidative stress resistance, and nutrient absorption into plants. It is unknown whether leaf and bract cell endosymbioses are significant in increasing the nitrogen content of plants. From the experiments that we conducted, it is impossible to know whether plant trichomes evolved specifically as organs for nitrogen fixation or if, instead, trichomes are structures in which bacteria easily colonize and where some casual nitrogen transfer may occur between bacteria and plant cells. It is likely that the endosymbioses seen in leaves and bracts are less efficient than those of root nodules of legumes in similar plants. However, the presence of endosymbioses that yield nitrate in plants could confer a reduced need for soil nitrogen and constitute increased nitrogen-use efficiency, even if the actual amount of nitrogen transferred to plant cells is small. More research is needed to evaluate the importance of nitrogen transfer within leaf and bract cells of plants. View Full-Text
Keywords: endophytes; histochemistry; nitrate; nitrogen-use efficiency; trichomes; nuclei; phyllosphere endophytes; histochemistry; nitrate; nitrogen-use efficiency; trichomes; nuclei; phyllosphere
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MDPI and ACS Style

Micci, A.; Zhang, Q.; Chang, X.; Kingsley, K.; Park, L.; Chiaranunt, P.; Strickland, R.; Velazquez, F.; Lindert, S.; Elmore, M.; Vines, P.L.; Crane, S.; Irizarry, I.; Kowalski, K.P.; Johnston-Monje, D.; White, J.F. Histochemical Evidence for Nitrogen-Transfer Endosymbiosis in Non-Photosynthetic Cells of Leaves and Inflorescence Bracts of Angiosperms. Biology 2022, 11, 876. https://doi.org/10.3390/biology11060876

AMA Style

Micci A, Zhang Q, Chang X, Kingsley K, Park L, Chiaranunt P, Strickland R, Velazquez F, Lindert S, Elmore M, Vines PL, Crane S, Irizarry I, Kowalski KP, Johnston-Monje D, White JF. Histochemical Evidence for Nitrogen-Transfer Endosymbiosis in Non-Photosynthetic Cells of Leaves and Inflorescence Bracts of Angiosperms. Biology. 2022; 11(6):876. https://doi.org/10.3390/biology11060876

Chicago/Turabian Style

Micci, April, Qiuwei Zhang, Xiaoqian Chang, Kathryn Kingsley, Linsey Park, Peerapol Chiaranunt, Raquele Strickland, Fernando Velazquez, Sean Lindert, Matthew Elmore, Philip L. Vines, Sharron Crane, Ivelisse Irizarry, Kurt P. Kowalski, David Johnston-Monje, and James F. White. 2022. "Histochemical Evidence for Nitrogen-Transfer Endosymbiosis in Non-Photosynthetic Cells of Leaves and Inflorescence Bracts of Angiosperms" Biology 11, no. 6: 876. https://doi.org/10.3390/biology11060876

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