Soil phosphorus availability alters the correlations between root phosphorus-uptake rates and net photosynthesis of dominant C
nonstructural carbohydrates
phosphorus (P) uptake
photosynthesis
rhizosheath soil
root functional traits
Journal
The New phytologist
ISSN: 1469-8137
Titre abrégé: New Phytol
Pays: England
ID NLM: 9882884
Informations de publication
Date de publication:
10 2023
10 2023
Historique:
received:
07
11
2022
accepted:
30
06
2023
medline:
8
9
2023
pubmed:
7
8
2023
entrez:
7
8
2023
Statut:
ppublish
Résumé
Phosphorus (P) fertilization can alleviate a soil P deficiency in grassland ecosystems. Understanding plant functional traits that enhance P uptake can improve grassland management. We measured impacts of P addition on soil chemical and microbial properties, net photosynthetic rate (P
Substances chimiques
Soil
0
Phosphorus
27YLU75U4W
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
157-172Informations de copyright
© 2023 The Authors New Phytologist © 2023 New Phytologist Foundation.
Références
Bai Y, Wu J, Clark CM, Naeem S, Pan Q, Huang J, Zhang L, Han X. 2010. Tradeoffs and thresholds in the effects of nitrogen addition on biodiversity and ecosystem functioning: evidence from inner Mongolia Grasslands. Global Change Biology 16: 358-372.
Bardgett RD, Mommer L, de Vries FT. 2014. Going underground: root traits as drivers of ecosystem processes. Trends in Ecology and Evolution 29: 692-699.
Bergmann J, Weigelt A, van der Plas F, Laughlin DC, Kuyper TW, Guerrero-Ramirez N, Valverde-Barrantes OJ, Bruelheide H, Freschet GT, Iversen CM et al. 2020. The fungal collaboration gradient dominates the root economics space in plants. Science Advances 6: eaba3756.
Bilyera N, Hummel C, Daudin G, Santangeli M, Zhang X, Santner J, Lippold E, Schlüter S, Bertrand I, Wenzel W et al. 2022. Co-localised phosphorus mobilization processes in the rhizosphere of field-grown maize jointly contribute to plant nutrition. Soil Biology and Biochemistry 165: 108497.
Bolan NS, Naidu R, Mahimairaja S, Baskaran S. 1994. Influence of low-molecular-weight organic acids on the solubilization of phosphates. Biology and Fertility of Soils 18: 311-319.
Bossio DA, Scow KM. 1998. Impacts of carbon and flooding on soil microbial communities: phospholipid fatty acid profiles and substrate utilization patterns. Microbial Ecology 35: 265-278.
Burton AL, Brown KM, Lynch JP. 2013. Phenotypic diversity of root anatomical and architectural traits in species. Crop Science 53: 1042-1055.
Chen X, Condron LM, Dunfield KE, Wakelin SA, Chen L. 2021. Impact of grassland afforestation with contrasting tree species on soil phosphorus fractions and alkaline phosphatase gene communities. Soil Biology and Biochemistry 159: 108274.
Cui H, Sun W, Delgado-Baquerizo M, Song W, Ma J, Wang K, Ling X. 2020. Phosphorus addition regulates the responses of soil multifunctionality to nitrogen over-fertilization in a temperate grassland. Plant and Soil 473: 73-87.
Da Silva S, Sbrissia A, Pereira L. 2015. Ecophysiology of C4 forage grasses-understanding plant growth for optimising their use and management. Agriculture 5: 598-625.
Daniel TC, Sharpley AN, Lemunyon JL. 1998. Agricultural phosphorus and eutrophication: a symposium overview. Journal of Environmental Quality 27: 251-257.
Daverede IC, Kravchenko AN, Hoeft RG, Nafziger ED, Bullock DG, Warren JJ, Gonzini LC. 2004. Phosphorus runoff from incorporated and surface-applied liquid swine manure and phosphorus fertilizer. Journal of Environmental Quality 33: 1535-1544.
De Bauw P, Vandamme E, Lupembe A, Mwakasege L, Senthilkumar K, Dramé KN, Merckx R. 2019. Anatomical root responses of rice to combined phosphorus and water stress-relations to tolerance and breeding opportunities. Functional Plant Biology 46: 1009-1022.
Dick WA, Cheng L, Wang P. 2000. Soil acid and alkaline phosphatase activity as pH adjustment indicators. Soil Biology and Biochemistry 32: 1915-1919.
Dybzinski R, Taylor N, Prosser M, Niosi O, Demo M, Kilbane E. 2021. Nitrogen, water, and phosphorus uptake as functions of fine root mass in greenhouse microcosms of Poa pratensis. Plant Ecology 222: 977-991.
Filippelli GM. 2008. The global phosphorus cycle: past, present, and future. Elements 4: 89-95.
Finzi AC, Abramoff RZ, Spiller KS, Brzostek ER, Darby BA, Kramer MA, Phillips RP. 2015. Rhizosphere processes are quantitatively important components of terrestrial carbon and nutrient cycles. Global Change Biology 21: 2082-2094.
Fitter AH, Graves JD, Watkins NK, Robinson D, Scrimgeour C. 1998. Carbon transfer between plants and its control in networks of arbuscular mycorrhizas. Functional Ecology 12: 406-412.
Freschet GT, Pagès L, Iversen CM, Comas LH, Rewald B, Roumet C, Klimešová J, Zadworny M, Poorter H, Postma JA et al. 2021. A starting guide to root ecology: strengthening ecological concepts and standardizing root classification, sampling, processing and trait measurements. New Phytologist 232: 973-1122.
Freschet GT, Roumet C. 2017. Sampling roots to capture plant and soil functions. Functional Ecology 31: 1506-1518.
Freschet GT, Roumet C, Comas LH, Weemstra M, Bengough AG, Rewald B, Bardgett RD, De Deyn GB, Johnson D, Klimešová J et al. 2020. Root traits as drivers of plant and ecosystem functioning: current understanding, pitfalls and future research needs. New Phytologist 232: 1123-1158.
Ghannoum O, Paul MJ, Ward JL, Beale MH, Corol D, Conroy JP. 2008. The sensitivity of photosynthesis to phosphorus deficiency differs between C3 and C4 tropical grasses. Functional Plant Biology 35: 213-221.
Guerrieria R, Belmecheri S, Ollinger SV, Asbjornsen H, Jennings K, Xiao J, Stocker BD, Martin M, Hollinger DY, Bracho-Garrillo R et al. 2019. Disentangling the role of photosynthesis and stomatal conductance on rising forest water-use efficiency. Proceedings of the National Academy of Sciences, USA 16: 16909-16914.
Hammond JP, White PJ. 2008. Sucrose transport in the phloem: integrating root responses to phosphorus starvation. Journal of Experimental Botany 59: 93-109.
Hammond JP, White PJ. 2011. Sugar signaling in root responses to low phosphorus availability. Plant Physiology 156: 1033-1040.
Harpole WS, Ngai JT, Cleland EE, Seabloom EW, Borer ET, Bracken MES, Elser JJ, Gruner DS, Hillebrand H, Shurin JB et al. 2011. Nutrient co-limitation of primary producer communities. Ecology Letters 14: 852-862.
Hartmann H, Ziegler W, Trumbore S. 2013. Lethal drought leads to reduction in nonstructural carbohydrates in Norway spruce tree roots but not in the canopy. Functional Ecology 27: 413-427.
He Y, Cheng W, Zhou L, Shao J, Liu H, Zhou H, Zhu K, Zhou X. 2020. Soil DOC release and aggregate disruption mediate rhizosphere priming effect on soil C decomposition. Soil Biology and Biochemistry 144: 107787.
Hedin LO, Vitousek PM, Matson PA. 2003. Nutrient losses over four million years of tropical forest development. Ecology 84: 2231-2255.
van der Heijden MGA. 2010. Mycorrhizal fungi reduce nutrient loss from model grassland ecosystems. Ecology 91: 1163-1171.
van der Heijden MGA, Martin FM, Selosse MA, Sanders IR. 2015. Mycorrhizal ecology and evolution: the past, the present, and the future. New Phytologist 205: 1406-1423.
Ho MD, Rosas JC, Brown KM, Lynch JP. 2005. Root architectural tradeoffs for water and phosphorus acquisition. Functional Plant Biology 32: 737-748.
Huang G, Hayes PE, Ryan MH, Pang J, Lambers H. 2017. Peppermint trees shift their phosphorus-acquisition strategy along a strong gradient of plant-available phosphorus by increasing their transpiration at very low phosphorus availability. Oecologia 185: 387-400.
Huang J, Hu B, Qi K, Chen W, Pang X, Bao W, Tian G. 2016. Effects of phosphorus addition on soil microbial biomass and community composition in a subalpine spruce plantation. European Journal of Soil Biology 72: 35-41.
Jia JQ, Dong YS, Qi YC, Peng Q, Liu XC, Sun LJ, Guo SF, He YL, Cao CC, Yan ZQ. 2016. Effects of water and nitrogen addition on vegetation carbon pools in a semi-arid temperate steppe. Journal of Forestry Research 27: 621-629.
Johnson JF, Allan DL, Vance CP, Weiblen G. 1996. Root carbon dioxide fixation by phosphorus-deficient Lupinus albus (contribution to organic acid exudation by proteoid roots). Plant Physiology 112: 19-30.
Jones DL. 1998. Organic acids in the rhizosphere-a critical review. Plant and Soil 205: 25-44.
Kong D, Fridley JD. 2019. Does plant biomass partitioning reflect energetic investments in carbon and nutrient foraging? Functional Ecology 33: 1627-1637.
Kong D, Wang J, Valverde-Barrantes OJ, Kardol P. 2020. A framework to assess the carbon supply-consumption balance in plant roots. New Phytologist 229: 659-664.
Kong D, Wang J, Wu H, Valverde-Barrantes OJ, Wang R, Zeng H, Kardol P, Zhang H, Feng Y. 2019. Nonlinearity of root trait relationships and the root economics spectrum. Nature Communications 10: 2203.
Kramer-Walter KR, Bellingham PJ, Millar TR, Smissen RD, Richardson SJ, Laughlin DC. 2016. Root traits are multidimensional: specific root length is independent from root tissue density and the plant economic spectrum. Journal of Ecology 104: 1299-1310.
Krueger ES, Ochsner TE, Levi MR, Basara JB, Snitker GJ, Wyatt BM. 2021. Grassland productivity estimates informed by soil moisture measurements: statistical and mechanistic approaches. Agronomy Journal 113: 3498-3517.
Lambers H, Hayes PE, Laliberté E, Oliveira RS, Turner BL. 2015. Leaf manganese accumulation and phosphorus-acquisition efficiency. Trends in Plant Science 20: 83-90.
Li L, Li SM, Sun JH, Zhou LL, Bao XG, Zhang HG, Zhang FS. 2007. Diversity enhances agricultural productivity via rhizosphere phosphorus facilitation on phosphorus-deficient soils. Proceedings of the National Academy of Sciences, USA 104: 11192-11196.
Li Y, Niu S, Yu GR. 2016. Aggravated phosphorus limitation on biomass production under increasing N addition: a meta-analysis. Global Change Biology 22: 934-943.
Lie Z, Zhou G, Huang W, Kadowaki K, Tissue DT, Yan J, Peñuelas J, Sardans J, Li Y, Liu S et al. 2022. Warming drives sustained plant phosphorus demand in a humid tropical forest. Global Change Biology 28: 4085-4096.
Liu Y, Zhang G, Luo X, Hou E, Zheng M, Zhang L, He X, Shen W, Wen D. 2021. Mycorrhizal fungi and phosphatase involvement in rhizosphere phosphorus transformations improves plant nutrition during subtropical forest succession. Soil Biology and Biochemistry 153: 108099.
Lu H, Huang Y, Qiao D, Han Y, Zhao Y, Bai F. 2021. Examination of Cd accumulation within sunflowers enhanced by low molecular weight organic acids in alkaline soil utilizing an improved Freundlich Model. Journal of Soil Science and Plant Nutrition 21: 2626-2641.
Luo Q, Gong J, Yang L, Li X, Pan Y, Liu M, Zhai Z, Baoyin T. 2017. Impacts of nitrogen addition on the carbon balance in a temperate semiarid grassland ecosystem. Biology and Fertility of Soils 53: 911-927.
Lynch J, Brown K. 2008. Root strategies for phosphorus acquisition. In: White P, Hammond J, eds. The ecophysiology of plant-phosphorus interaction, vol. 7. Berlin, Germany: Springer, 83-116.
Lynch JP. 2011. Root phenes for enhanced soil exploration and phosphorus acquisition: tools for future crops. Plant Physiology 156: 1041-1049.
Lynch JP, Ho MD. 2005. Rhizoeconomics: carbon costs of phosphorus acquisition. Plant and Soil 269: 45-56.
Matzek V. 2012. Trait values, not trait plasticity, best explain invasive species' performance in a changing environment. PLoS ONE 7: e48821.
Newman EI. 1995. Phosphorus inputs to terrestrial ecosystems. Journal of Ecology 83: 713-726.
Okamoto H, Kitamura S, Masaki N. 2022. Activation of the root xylem proton pump by hydraulic signals from leaves under suppressed transpiration. Journal of Plant Research 135: 311-322.
Pang J, Bansal R, Zhao H, Bohuon E, Lambers H, Ryan MH, Ranathunge K, Siddique KMH. 2018. The carboxylate-releasing phosphorus-mobilising strategy could be proxied by foliar manganese concentration in a large set of chickpea germplasm under low phosphorus supply. New Phytologist 219: 518-529.
Pastore MA, Lee TD, Hobbie SE, Reich PB. 2019. Strong photosynthetic acclimation and enhanced water-use efficiency in grassland functional groups persist over 21 years of CO2 enrichment, independent of nitrogen supply. Global Change Biology 25: 3031-3044.
Pregitzer KS. 2002. Fine roots of trees-a new perspective. New Phytologist 154: 267-270.
Prescott CE. 2022. Sinks for plant surplus carbon explain several ecological phenomena. Plant and Soil 476: 689-698.
Prescott CE, Grayston SJ, Helmisaari HS, Kaštovská E, Körner C, Lambers H, Meier IC, Millard P, Ostonen I. 2020. Surplus carbon drives allocation and plant-soil interactions. Trends in Ecology & Evolution 35: 1110-1118.
Qiu H, Liu C, Yu T, Mei X, Wang G, Wang J, Cai Y. 2014. Identification of QTL for acid phosphatase activity in root and rhizosphere soil of maize under low phosphorus stress. Euphytica 197: 133-143.
Raven JA, Lambers H, Smith SE, Westoby M. 2018. Costs of acquiring phosphorus by vascular land plants: patterns and implications for plant coexistence. New Phytologist 217: 1420-1427.
Reich PB. 2014. The world-wide ‘fast-slow’ plant economics spectrum: a traits manifesto. Journal of Ecology 102: 275-301.
Reich PB, Wright IJ, Cavender-Bares JC, Craine M, Oleksyn J, Walters MB. 2003. The evolution of plant functional variation: traits, spectra, and strategies. International Journal of Plant Sciences 164: S143-S164.
Robinson D. 2010. The responses of plants to non-uniform supplies of nutrients. New Phytologist 127: 635-674.
Roumet C, Birouste M, Picon-Cochard C, Ghestem M, Osman N, Vrignon-Brenas S, Cao K, Stokes A. 2016. Root structure-function relationships in 74 species: evidence of a root economics spectrum related to carbon economy. New Phytologist 210: 815-826.
Sage RF, Wedin DA, Li M. 1999. The biogeography of C4 photosynthesis: patterns and controlling factors. In: Sage RF, Monson RK, eds. C4 plant biology. New York, NY, USA: Academic Press, 313-373.
Sattari SZ, Bouwman AF, Martinez Rodríguez R, Beusen AHW, van Ittersum MK. 2016. Negative global phosphorus budgets challenge sustainable intensification of grasslands. Nature Communications 7: 10696.
Sheng M, Lalande R, Hamel C, Ziadi N, Shi Y. 2012. Growth of corn roots and associated arbuscular mycorrhizae are affected by long-term tillage and phosphorus fertilization. Agronomy Journal 104: 1672-1678.
Shi J, Gong J, Baoyin T, Luo Q, Zhai Z, Zhu C, Yang B, Wang B, Zhang Z, Li X. 2021. Short-term phosphorus addition increases soil respiration by promoting gross ecosystem production and litter decomposition in a typical temperate grassland in northern China. Catena 197: 104952.
Shi J, Gong J, Li X, Zhang Z, Zhang W, Li Y, Song L, Zhang S, Dong J, Baoyin T. 2022. Plant-microbial linkages regulate soil organic carbon dynamics under phosphorus application in a typical temperate grassland in northern China. Agriculture, Ecosystems and Environment 335: 108006.
Song L, Gong J, Li X, Ding Y, Shi J, Zhang Z, Zhang W, Li Y, Zhang S, Dong J. 2022. Plant phosphorus demand stimulates rhizosphere phosphorus transition byroot exudates and mycorrhizal fungi under different grazing intensities. Geoderma 423: 115964.
Strobel BW. 2001. Influence of vegetation on low-molecular-weight carboxylic acids in soil solution-a review. Geoderma 99: 169-198.
Tian Q, Liu N, Ma P, Zhou H, Zhai X, Chen M, Wang H, Li W, Bai W, Lambers H et al. 2021. Processes at the soil-root interface determine the different responses of nutrient limitation and metal toxicity in forbs and grasses to nitrogen enrichment. Journal of Ecology 109: 927-938.
Ven A, Verlinden MS, Vebruggen E, Vicca S. 2019. Experimental evidence that phosphorus fertilization and arbuscular mycorrhizal symbiosis can reduce the carbon cost of phosphorus uptake. Functional Ecology 33: 1-11.
Vitousek PM, Porder S, Houlton BZ, Chadwick OA. 2010. Terrestrial phosphorus limitation: mechanisms, implications, and nitrogen-phosphorus interactions. Ecological Applications 20: 5-15.
Wang B, Gong J, Zhang Z, Yang B, Liu M, Zhu C. 2019. Nitrogen addition alters photosynthetic carbon fixation, allocation of photoassimilates, and carbon partitioning of Leymus chinensis in a temperate grassland of Inner Mongolia. Agricultural and Forest Meteorology 279: 107743.
Wang H, Liu S, Zhang X, Mao Q, Li X, You Y, Wang J, Zheng M, Zhang W, Lu X et al. 2018. Nitrogen addition reduces soil bacterial richness, while phosphorus addition alters community composition in an old-growth N-rich tropical forest in southern China. Soil Biology and Biochemistry 127: 22-30.
Wang JH, Wang SP, Schnug E, Haneklaus S, Patton B, Nyren P. 2008. Competition between Stipa grandis and Cleistogenes squarrosa. Journal of Arid Environments 72: 63-72.
Wei K, Sun T, Tian JH, Chen ZH, Chen LJ. 2018. Soil microbial biomass, phosphatase and their relationships with phosphorus turnover under mixed inorganic and organic nitrogen addition in a Larix gmelinii plantation. Forest Ecology and Management 422: 313-322.
Wen Z, White PJ, Shen J, Lambers H. 2021. Linking root exudation to belowground economic traits for resource acquisition. New Phytologist 233: 1620-1635.
Wright JP, Ames GM, Mitchell RM. 2016. The more things change, the more they stay the same? When is trait variability important for stability of ecosystem function in a changing environment. Philosophical Transactions of the Royal Society B: Biological Sciences 371: 20150272.
Yin H, Li Y, Xiao J, Xu Z, Cheng X, Liu Q. 2013. Enhanced root exudation stimulates soil nitrogen transformations in a subalpine coniferous forest under experimental warming. Global Change Biology 19: 2158-2167.
Yu R-P, Li XX, Xiao ZH, Lambers H, Li L. 2020. Phosphorus facilitation and covariation of root traits in steppe species. New Phytologist 226: 1285-1298.
Zemunik G, Turner BL, Lambers H, Laliberté E. 2015. Diversity of plant nutrient-acquisition strategies increases during long-term ecosystem development. Nature Plants 1: 15050.
Zeng F, Chen S, Miao Y, Wu F, Zhang G. 2008. Changes of organic acid exudation and rhizosphere pH in rice plants under chromium stress. Environmental Pollution 155: 284-289.
Zhao Y, Ma J, Sun X, Guo X. 2014. Spatial distribution of soil moisture and fine roots of apple trees under water storage pit irrigation. Journal of Irrigation and Drainage Engineering 140: 6013001.
Zhou M, Guo Y, Sheng J, Yuan Y, Zhang WH, Bai W. 2022. Using anatomical traits to understand root functions across root orders of herbaceous species in a temperate steppe. New Phytologist 234: 422-434.
Zhou T, Wang L, Sun X, Wang X, Chen Y, Rengel Z, Liu W, Yang W. 2019. Light intensity influence maize adaptation to low P stress by altering root morphology. Plant and Soil 447: 183-197.