Nitrate is an important nitrogen source for Arctic tundra plants

Xue Yan Liu; Keisuke Koba; Lina A. Koyama; Sarah E. Hobbie; Marissa S. Weiss; Yoshiyuki Inagaki; Gaius R. Shaver; Anne E. Giblin; Satoru Hobara; Knute J. Nadelhoffer; Martin Sommerkorn; Edward B. Rastetter; George W. Kling; James A. Laundre; Yuriko Yano; Akiko Makabe; Midori Yano; Cong Qiang Liu

doi:10.1073/pnas.1715382115

Nitrate is an important nitrogen source for Arctic tundra plants

Xue Yan Liu, Keisuke Koba, Lina A. Koyama, Sarah E. Hobbie, Marissa S. Weiss, Yoshiyuki Inagaki, Gaius R. Shaver, Anne E. Giblin, Satoru Hobara, Knute J. Nadelhoffer, Martin Sommerkorn, Edward B. Rastetter, George W. Kling, James A. Laundre, Yuriko Yano, Akiko Makabe, Midori Yano, Cong Qiang Liu

Ecology, Evolution and Behavior

Research output: Contribution to journal › Article › peer-review

108 Scopus citations

Abstract

Plant nitrogen (N) use is a key component of the N cycle in terrestrial ecosystems. The supply of N to plants affects community species composition and ecosystem processes such as photosynthesis and carbon (C) accumulation. However, the availabilities and relative importance of different N forms to plants are not well understood. While nitrate (NO₃ ⁻) is a major N form used by plants worldwide, it is discounted as a N source for Arctic tundra plants because of extremely low NO₃ ⁻ concentrations in Arctic tundra soils, undetectable soil nitrification, and plant-tissue NO₃ ⁻ that is typically below detection limits. Here we reexamine NO₃ ⁻ use by tundra plants using a sensitive denitrifier method to analyze plant-tissue NO₃ ⁻. Soil-derived NO₃ ⁻ was detected in tundra plant tissues, and tundra plants took up soil NO₃ ⁻ at comparable rates to plants from relatively NO₃ ⁻-rich ecosystems in other biomes. Nitrate assimilation determined by¹⁵N enrichments of leaf NO₃ ⁻ relative to soil NO₃ ⁻ accounted for 4 to 52% (as estimated by a Bayesian isotope-mixing model) of species-specific total leaf N of Alaskan tundra plants. Our finding that in situ soil NO₃ ⁻ availability for tundra plants is high has important implications for Arctic ecosystems, not only in determining species compositions, but also in determining the loss of N from soils via leaching and denitrification. Plant N uptake and soil N losses can strongly influence C uptake and accumulation in tundra soils. Accordingly, this evidence of NO₃ ⁻ availability in tundra soils is crucial for predicting C storage in tundra.

Original language	English (US)
Pages (from-to)	3398-3403
Number of pages	6
Journal	Proceedings of the National Academy of Sciences of the United States of America
Volume	115
Issue number	13
DOIs	https://doi.org/10.1073/pnas.1715382115
State	Published - Mar 27 2018

Bibliographical note

Funding Information:
We thank Laura Gough, Andrew J. Schauer, Muneoki Yoh, Nozomi Suzuki, Naohiro Yoshida, Yanbao Lei, Xiaodong Li, Erica Steve, Marshall Otter, Asami Nakanishi, Takahiro Hayashi, Ryo Kobayashi, Chieko Takahashi, Syuichiro Matsushima, Hiroyu Katoh, Azusa A. Hokari, Tomoko Makita, and colleagues and staff at TFS, TUAT, Center for Ecological Research, and the Institute of Geochemistry, Chinese Academy of Sciences for their assistance in the field and laboratory. We also thank Hideo Yamasaki for fruitful discussions on NO3− production by plants, and Erik Hobbie for helpful comments during the revision. This study was supported by the Kyoto University Foundation, the Sumitomo Foundation, Program for Next Generation World-Leading Researcher (Grant GS008) and Grant-in-Aid for Scientific Research (KAKENHI Grants 26252020, 26550004, 17H06297, and P09316) from the Japan Society for Promotion of Science, the National Natural Science Foundation of China (Grants 41730855, 41522301, and 41473081), the National Key Research and Development Program of China (Grants 2016YFA0600802 and 2017YFC0210101), and the 11th Recruitment Program of Global Experts (the Thousand Talents Plan) for Young Professionals granted by the central budget of China. Logistical support at Toolik Lake was provided by the US National Science Foundation Office of Polar Programs. Site selection, site maintenance, site descriptions, and field data were provided by the Arctic Long-Term Ecological Research program, funded by the US National Science Foundation Division of Environmental Biology (Grants 1026843, 1504006, and 1637459).

Funding Information:
ACKNOWLEDGMENTS. We thank Laura Gough, Andrew J. Schauer, Muneoki Yoh, Nozomi Suzuki, Naohiro Yoshida, Yanbao Lei, Xiaodong Li, Erica Steve, Marshall Otter, Asami Nakanishi, Takahiro Hayashi, Ryo Kobayashi, Chieko Takahashi, Syuichiro Matsushima, Hiroyu Katoh, Azusa A. Hokari, Tomoko Makita, and colleagues and staff at TFS, TUAT, Center for Ecological Research, and the Institute of Geochemistry, Chinese Academy of Sciences for their assistance in the field and laboratory. We also thank Hideo Yamasaki for fruitful discussions on NO3− production by plants, and Erik Hobbie for helpful comments during the revision. This study was supported by the Kyoto University Foundation, the Sumitomo Foundation, Program for Next Generation World-Leading Researcher (Grant GS008) and Grant-in-Aid for Scientific Research (KAKENHI Grants 26252020, 26550004, 17H06297, and P09316) from the Japan Society for Promotion of Science, the National Natural Science Foundation of China (Grants 41730855, 41522301, and 41473081), the National Key Research and Development Program of China (Grants 2016YFA0600802 and 2017YFC0210101), and the 11th Recruitment Program of Global Experts (the Thousand Talents Plan) for Young Professionals granted by the central budget of China. Logistical support at Toolik Lake was provided by the US National Science Foundation Office of Polar Programs. Site selection, site maintenance, site descriptions, and field data were provided by the Arctic Long-Term Ecological Research program, funded by the US National Science Foundation Division of Environmental Biology (Grants 1026843, 1504006, and 1637459).

Publisher Copyright:
© 2018 National Academy of Sciences. All Rights Reserved.

Keywords

Arctic tundra plants
Nitrogen dynamics
Plant nitrate
Soil nitrate
Stable isotopes

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10.1073/pnas.1715382115

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Liu, X. Y., Koba, K., Koyama, L. A., Hobbie, S. E., Weiss, M. S., Inagaki, Y., Shaver, G. R., Giblin, A. E., Hobara, S., Nadelhoffer, K. J., Sommerkorn, M., Rastetter, E. B., Kling, G. W., Laundre, J. A., Yano, Y., Makabe, A., Yano, M., & Liu, C. Q. (2018). Nitrate is an important nitrogen source for Arctic tundra plants. Proceedings of the National Academy of Sciences of the United States of America, 115(13), 3398-3403. https://doi.org/10.1073/pnas.1715382115

Liu, XY, Koba, K, Koyama, LA, Hobbie, SE, Weiss, MS, Inagaki, Y, Shaver, GR, Giblin, AE, Hobara, S, Nadelhoffer, KJ, Sommerkorn, M, Rastetter, EB, Kling, GW, Laundre, JA, Yano, Y, Makabe, A, Yano, M & Liu, CQ 2018, 'Nitrate is an important nitrogen source for Arctic tundra plants', Proceedings of the National Academy of Sciences of the United States of America, vol. 115, no. 13, pp. 3398-3403. https://doi.org/10.1073/pnas.1715382115

@article{2950fdb5c1904569a78a6da3b4f7b986,

title = "Nitrate is an important nitrogen source for Arctic tundra plants",

abstract = "Plant nitrogen (N) use is a key component of the N cycle in terrestrial ecosystems. The supply of N to plants affects community species composition and ecosystem processes such as photosynthesis and carbon (C) accumulation. However, the availabilities and relative importance of different N forms to plants are not well understood. While nitrate (NO3 −) is a major N form used by plants worldwide, it is discounted as a N source for Arctic tundra plants because of extremely low NO3 − concentrations in Arctic tundra soils, undetectable soil nitrification, and plant-tissue NO3 − that is typically below detection limits. Here we reexamine NO3 − use by tundra plants using a sensitive denitrifier method to analyze plant-tissue NO3 −. Soil-derived NO3 − was detected in tundra plant tissues, and tundra plants took up soil NO3 − at comparable rates to plants from relatively NO3 −-rich ecosystems in other biomes. Nitrate assimilation determined by15N enrichments of leaf NO3 − relative to soil NO3 − accounted for 4 to 52% (as estimated by a Bayesian isotope-mixing model) of species-specific total leaf N of Alaskan tundra plants. Our finding that in situ soil NO3 − availability for tundra plants is high has important implications for Arctic ecosystems, not only in determining species compositions, but also in determining the loss of N from soils via leaching and denitrification. Plant N uptake and soil N losses can strongly influence C uptake and accumulation in tundra soils. Accordingly, this evidence of NO3 − availability in tundra soils is crucial for predicting C storage in tundra.",

keywords = "Arctic tundra plants, Nitrogen dynamics, Plant nitrate, Soil nitrate, Stable isotopes",

author = "Liu, {Xue Yan} and Keisuke Koba and Koyama, {Lina A.} and Hobbie, {Sarah E.} and Weiss, {Marissa S.} and Yoshiyuki Inagaki and Shaver, {Gaius R.} and Giblin, {Anne E.} and Satoru Hobara and Nadelhoffer, {Knute J.} and Martin Sommerkorn and Rastetter, {Edward B.} and Kling, {George W.} and Laundre, {James A.} and Yuriko Yano and Akiko Makabe and Midori Yano and Liu, {Cong Qiang}",

note = "Funding Information: We thank Laura Gough, Andrew J. Schauer, Muneoki Yoh, Nozomi Suzuki, Naohiro Yoshida, Yanbao Lei, Xiaodong Li, Erica Steve, Marshall Otter, Asami Nakanishi, Takahiro Hayashi, Ryo Kobayashi, Chieko Takahashi, Syuichiro Matsushima, Hiroyu Katoh, Azusa A. Hokari, Tomoko Makita, and colleagues and staff at TFS, TUAT, Center for Ecological Research, and the Institute of Geochemistry, Chinese Academy of Sciences for their assistance in the field and laboratory. We also thank Hideo Yamasaki for fruitful discussions on NO3− production by plants, and Erik Hobbie for helpful comments during the revision. This study was supported by the Kyoto University Foundation, the Sumitomo Foundation, Program for Next Generation World-Leading Researcher (Grant GS008) and Grant-in-Aid for Scientific Research (KAKENHI Grants 26252020, 26550004, 17H06297, and P09316) from the Japan Society for Promotion of Science, the National Natural Science Foundation of China (Grants 41730855, 41522301, and 41473081), the National Key Research and Development Program of China (Grants 2016YFA0600802 and 2017YFC0210101), and the 11th Recruitment Program of Global Experts (the Thousand Talents Plan) for Young Professionals granted by the central budget of China. Logistical support at Toolik Lake was provided by the US National Science Foundation Office of Polar Programs. Site selection, site maintenance, site descriptions, and field data were provided by the Arctic Long-Term Ecological Research program, funded by the US National Science Foundation Division of Environmental Biology (Grants 1026843, 1504006, and 1637459). Funding Information: ACKNOWLEDGMENTS. We thank Laura Gough, Andrew J. Schauer, Muneoki Yoh, Nozomi Suzuki, Naohiro Yoshida, Yanbao Lei, Xiaodong Li, Erica Steve, Marshall Otter, Asami Nakanishi, Takahiro Hayashi, Ryo Kobayashi, Chieko Takahashi, Syuichiro Matsushima, Hiroyu Katoh, Azusa A. Hokari, Tomoko Makita, and colleagues and staff at TFS, TUAT, Center for Ecological Research, and the Institute of Geochemistry, Chinese Academy of Sciences for their assistance in the field and laboratory. We also thank Hideo Yamasaki for fruitful discussions on NO3− production by plants, and Erik Hobbie for helpful comments during the revision. This study was supported by the Kyoto University Foundation, the Sumitomo Foundation, Program for Next Generation World-Leading Researcher (Grant GS008) and Grant-in-Aid for Scientific Research (KAKENHI Grants 26252020, 26550004, 17H06297, and P09316) from the Japan Society for Promotion of Science, the National Natural Science Foundation of China (Grants 41730855, 41522301, and 41473081), the National Key Research and Development Program of China (Grants 2016YFA0600802 and 2017YFC0210101), and the 11th Recruitment Program of Global Experts (the Thousand Talents Plan) for Young Professionals granted by the central budget of China. Logistical support at Toolik Lake was provided by the US National Science Foundation Office of Polar Programs. Site selection, site maintenance, site descriptions, and field data were provided by the Arctic Long-Term Ecological Research program, funded by the US National Science Foundation Division of Environmental Biology (Grants 1026843, 1504006, and 1637459). Publisher Copyright: {\textcopyright} 2018 National Academy of Sciences. All Rights Reserved.",

year = "2018",

month = mar,

day = "27",

doi = "10.1073/pnas.1715382115",

language = "English (US)",

volume = "115",

pages = "3398--3403",

journal = "Proceedings of the National Academy of Sciences of the United States of America",

issn = "0027-8424",

publisher = "National Academy of Sciences",

number = "13",

}

TY - JOUR

T1 - Nitrate is an important nitrogen source for Arctic tundra plants

AU - Liu, Xue Yan

AU - Koba, Keisuke

AU - Koyama, Lina A.

AU - Hobbie, Sarah E.

AU - Weiss, Marissa S.

AU - Inagaki, Yoshiyuki

AU - Shaver, Gaius R.

AU - Giblin, Anne E.

AU - Hobara, Satoru

AU - Nadelhoffer, Knute J.

AU - Sommerkorn, Martin

AU - Rastetter, Edward B.

AU - Kling, George W.

AU - Laundre, James A.

AU - Yano, Yuriko

AU - Makabe, Akiko

AU - Yano, Midori

AU - Liu, Cong Qiang

N1 - Funding Information: We thank Laura Gough, Andrew J. Schauer, Muneoki Yoh, Nozomi Suzuki, Naohiro Yoshida, Yanbao Lei, Xiaodong Li, Erica Steve, Marshall Otter, Asami Nakanishi, Takahiro Hayashi, Ryo Kobayashi, Chieko Takahashi, Syuichiro Matsushima, Hiroyu Katoh, Azusa A. Hokari, Tomoko Makita, and colleagues and staff at TFS, TUAT, Center for Ecological Research, and the Institute of Geochemistry, Chinese Academy of Sciences for their assistance in the field and laboratory. We also thank Hideo Yamasaki for fruitful discussions on NO3− production by plants, and Erik Hobbie for helpful comments during the revision. This study was supported by the Kyoto University Foundation, the Sumitomo Foundation, Program for Next Generation World-Leading Researcher (Grant GS008) and Grant-in-Aid for Scientific Research (KAKENHI Grants 26252020, 26550004, 17H06297, and P09316) from the Japan Society for Promotion of Science, the National Natural Science Foundation of China (Grants 41730855, 41522301, and 41473081), the National Key Research and Development Program of China (Grants 2016YFA0600802 and 2017YFC0210101), and the 11th Recruitment Program of Global Experts (the Thousand Talents Plan) for Young Professionals granted by the central budget of China. Logistical support at Toolik Lake was provided by the US National Science Foundation Office of Polar Programs. Site selection, site maintenance, site descriptions, and field data were provided by the Arctic Long-Term Ecological Research program, funded by the US National Science Foundation Division of Environmental Biology (Grants 1026843, 1504006, and 1637459). Funding Information: ACKNOWLEDGMENTS. We thank Laura Gough, Andrew J. Schauer, Muneoki Yoh, Nozomi Suzuki, Naohiro Yoshida, Yanbao Lei, Xiaodong Li, Erica Steve, Marshall Otter, Asami Nakanishi, Takahiro Hayashi, Ryo Kobayashi, Chieko Takahashi, Syuichiro Matsushima, Hiroyu Katoh, Azusa A. Hokari, Tomoko Makita, and colleagues and staff at TFS, TUAT, Center for Ecological Research, and the Institute of Geochemistry, Chinese Academy of Sciences for their assistance in the field and laboratory. We also thank Hideo Yamasaki for fruitful discussions on NO3− production by plants, and Erik Hobbie for helpful comments during the revision. This study was supported by the Kyoto University Foundation, the Sumitomo Foundation, Program for Next Generation World-Leading Researcher (Grant GS008) and Grant-in-Aid for Scientific Research (KAKENHI Grants 26252020, 26550004, 17H06297, and P09316) from the Japan Society for Promotion of Science, the National Natural Science Foundation of China (Grants 41730855, 41522301, and 41473081), the National Key Research and Development Program of China (Grants 2016YFA0600802 and 2017YFC0210101), and the 11th Recruitment Program of Global Experts (the Thousand Talents Plan) for Young Professionals granted by the central budget of China. Logistical support at Toolik Lake was provided by the US National Science Foundation Office of Polar Programs. Site selection, site maintenance, site descriptions, and field data were provided by the Arctic Long-Term Ecological Research program, funded by the US National Science Foundation Division of Environmental Biology (Grants 1026843, 1504006, and 1637459). Publisher Copyright: © 2018 National Academy of Sciences. All Rights Reserved.

PY - 2018/3/27

Y1 - 2018/3/27

N2 - Plant nitrogen (N) use is a key component of the N cycle in terrestrial ecosystems. The supply of N to plants affects community species composition and ecosystem processes such as photosynthesis and carbon (C) accumulation. However, the availabilities and relative importance of different N forms to plants are not well understood. While nitrate (NO3 −) is a major N form used by plants worldwide, it is discounted as a N source for Arctic tundra plants because of extremely low NO3 − concentrations in Arctic tundra soils, undetectable soil nitrification, and plant-tissue NO3 − that is typically below detection limits. Here we reexamine NO3 − use by tundra plants using a sensitive denitrifier method to analyze plant-tissue NO3 −. Soil-derived NO3 − was detected in tundra plant tissues, and tundra plants took up soil NO3 − at comparable rates to plants from relatively NO3 −-rich ecosystems in other biomes. Nitrate assimilation determined by15N enrichments of leaf NO3 − relative to soil NO3 − accounted for 4 to 52% (as estimated by a Bayesian isotope-mixing model) of species-specific total leaf N of Alaskan tundra plants. Our finding that in situ soil NO3 − availability for tundra plants is high has important implications for Arctic ecosystems, not only in determining species compositions, but also in determining the loss of N from soils via leaching and denitrification. Plant N uptake and soil N losses can strongly influence C uptake and accumulation in tundra soils. Accordingly, this evidence of NO3 − availability in tundra soils is crucial for predicting C storage in tundra.

AB - Plant nitrogen (N) use is a key component of the N cycle in terrestrial ecosystems. The supply of N to plants affects community species composition and ecosystem processes such as photosynthesis and carbon (C) accumulation. However, the availabilities and relative importance of different N forms to plants are not well understood. While nitrate (NO3 −) is a major N form used by plants worldwide, it is discounted as a N source for Arctic tundra plants because of extremely low NO3 − concentrations in Arctic tundra soils, undetectable soil nitrification, and plant-tissue NO3 − that is typically below detection limits. Here we reexamine NO3 − use by tundra plants using a sensitive denitrifier method to analyze plant-tissue NO3 −. Soil-derived NO3 − was detected in tundra plant tissues, and tundra plants took up soil NO3 − at comparable rates to plants from relatively NO3 −-rich ecosystems in other biomes. Nitrate assimilation determined by15N enrichments of leaf NO3 − relative to soil NO3 − accounted for 4 to 52% (as estimated by a Bayesian isotope-mixing model) of species-specific total leaf N of Alaskan tundra plants. Our finding that in situ soil NO3 − availability for tundra plants is high has important implications for Arctic ecosystems, not only in determining species compositions, but also in determining the loss of N from soils via leaching and denitrification. Plant N uptake and soil N losses can strongly influence C uptake and accumulation in tundra soils. Accordingly, this evidence of NO3 − availability in tundra soils is crucial for predicting C storage in tundra.

KW - Arctic tundra plants

KW - Nitrogen dynamics

KW - Plant nitrate

KW - Soil nitrate

KW - Stable isotopes

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U2 - 10.1073/pnas.1715382115

DO - 10.1073/pnas.1715382115

M3 - Article

C2 - 29540568

AN - SCOPUS:85044420119

SN - 0027-8424

VL - 115

SP - 3398

EP - 3403

JO - Proceedings of the National Academy of Sciences of the United States of America

JF - Proceedings of the National Academy of Sciences of the United States of America

IS - 13

ER -

Nitrate is an important nitrogen source for Arctic tundra plants

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