Abstract
Carbon (C) allocation plays a vital role in enabling plants to effectively cope with limited phosphorus (P) availability, especially in P-deficient subtropic. However, in what pattern did C allocated to different plant organs along a P gradient is still unclear. This study conducted a nutrient manipulation experiment on Pinus massoniana seedlings, an endemic species in subtropical China, to explore the variations in non-structural carbohydrate (NSC) fractions of needles and roots along a fact-based P gradient of 0–9.299 mg·kg−1 (0–4 times of average soil available P content in the major distribution area of P. massoniana). P promoted the relative growth rate of P. massoniana seedlings. Biomass showed no difference along the P gradient, but biomass proportion of fine root decreased with P addition. The C concentration in new needle increased with increasing substrate P content, but old needle showed an reverse trend. Old needle remained major C pool in low-P conditions, but more C would be allocated to new needle with P addition. Higher C was found in fine root in low-P groups. The NSC concentration in needles rose with P addition, but decreased in roots. NSC existed more in the form of soluble sugar in needles in low-P conditions, but more in the form of starch in fine root. In low-P conditions, P. massoniana seedlings regulated growth by preferentially allocating C to fine root and old needle, promoting absorption and maintaining a stable C pool, while exhibiting distinct NSC fraction patterns in fine root (starch) and needles (soluble sugar).
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Data Availability
The datasets used in the current study are available from the corresponding author on reasonable request.
References
Alvarez-Clare S, Mack MC, Brooks ME (2013) A direct test of nitrogen and phosphorus limitation to net primary productivity in a lowland tropical wet forest. Ecology 94:1540–1551. https://doi.org/10.1890/12-2128.1
Chai YN, Schachtman DP (2020) Root exudates impact plant performance under abiotic stress. Trends Plant Sci 27:80–91. https://doi.org/10.1016/j.tplants.2021.08.003
Chapin FS (1990) The ecology and economics of storage in plants. Annu Rev Ecol Syst 21:423–447. https://doi.org/10.1146/annurev.ecolsys.21.1.423
Charles LS, Dwyer JM, Smith TJ, Connors S, Marschner P, Mayfield MM (2018) Seedling growth responses to species-, neighborhood-, and landscape-scale effects during tropical forest restoration. Ecosphere 9:e02386. https://doi.org/10.1002/ecs2.2386
Deng Q, Hui DF, Dennis S, Reddy KC (2017) Responses of terrestrial ecosystem phosphorus cycling to nitrogen addition: a meta-analysis. Glob Ecol Biogeogr 26:713–728. https://doi.org/10.1111/geb.12576
Deng XX, Shi Z, Zeng LX, Lei L, Xin XB, Pei SX, Xiao WF (2021) Photosynthetic product allocations to the organs of Pinus massoniana are not affected by differences in synthesis or temporal variations in translocation rates. Forests 12:471. https://doi.org/10.3390/f12040471
Dubois M, Gilles KA, Hamilton JK, Rebers PT, Smith F (1956) Colorimetric method for determination of sugars and related substances. Anal Chem 28:350–356. https://doi.org/10.1021/AC60111A017
Epstein E, Bloom AJ (1972) Mineral nutrition of plants: principles and perspectives. John Wiley and Sons, New York
Fletcher DMM, Ruiz S, Dias T, Petroselli C, Roose T (2020) Linking root structure to functionality: the impact of root system architecture on citrate-enhanced phosphate uptake. New Phytol 227:376–391. https://doi.org/10.1111/nph.16554
Freschet GT, Roumet C, Comas LH, Weemstra M, Bengough AG, Rewald B, Bardgett RD, De Deyn GB, Johnson D, Klimešová J, Lukac M, McCormack ML, Meier IC, Pagès L, Poorter H, Prieto I, Wurzburger N, Zadworny M, Bagniewska-Zadworna A, Blancaflor EB, Brunner I, Gessler A, Hobbie SE, Iversen CM, Mommer L, Picon-Cochard C, Postma JA, Rose L, Ryser P, Scherer-Lorenzen M, Soudzilovskaia NA, Sun T, Valverde-Barrantes OJ, Weigelt A, York LM, Stokes A (2020) Root traits as drivers of plant and ecosystem functioning: current understanding, pitfalls and future research needs. New Phytol 232:1123–1158. https://doi.org/10.1111/nph.17072
Gao WQ, Liu JF, Xue ZM, Zhang YT, Gao ZH, Ni YY, Wang XF, Jiang ZP (2018) Geographical patterns and drivers of growth dynamics of Quercus variabilis. For Ecol Manage 429:256–266. https://doi.org/10.1016/j.foreco.2018.07.024
Grau O, Peñuelas J, Ferry B, Freycon V, Blanc L, Desprez M, Baraloto C, Chave J, Descroix L, Dourdain A, Guitet S, Janssens IA, Sardans J, Hérault B (2017) Nutrient-cycling mechanisms other than the direct absorption from soil may control forest structure and dynamics in poor Amazonian soils. Sci Rep 7:1–11. https://doi.org/10.1038/srep45017
Huang X, Huang CB, Teng MJ, Zhou ZX, Wang PC (2020) Net primary productivity of Pinus massoniana dependence on climate, soil and forest characteristics. Forests 11:404. https://doi.org/10.3390/f11040404
Jackson RB, Mooney HA, Schulze ED (1997) A global budget for fine root biomass, surface area, and nutrient contents. Proc Natl Acad Sci U S A 94:7362–7366. https://doi.org/10.1073/pnas.94.14.7362
Jian ZJ, Ni YY, Xu J, Lei L, Zeng LX, Xiao WF (2021) Soil fertility in the Pinus massoniana forests of China. Acta Ecol Sin 41:5279–5288. https://doi.org/10.5846/stxb202007021716
Jian ZJ, Ni YY, Lei L, Xu J, Xiao WF, Zeng LX (2022) Phosphorus is the key soil indicator controlling productivity in planted Masson pine forests across subtropical China. Sci Total Environ 822:153525. https://doi.org/10.1016/j.scitotenv.2022.153525
Keith K, Raison RJ, Jacobsen KL (1997) Allocation of carbon in a mature eucalypt forest and some effects of soil phosphorus availability. Plant Soil 196:81–99. https://doi.org/10.1023/A:1004286030345
Laliberté E, Lambers H, Burgess TI, Wright SJ (2014) Phosphorus limitation, soil-borne pathogens and the coexistence of plant species in hyperdiverse forests and shrublands. New Phytol 206:507–521. https://doi.org/10.1111/nph.13203
Lambers H, Clements JC, Nelson MN (2013) How a phosphorus-acquisition strategy based on carboxylate exudation powers the success and agronomic potential of lupines (Lupinus, Fabaceae). Am J Bot 100:263–288. https://doi.org/10.3732/ajb.1200474
Li Y, Tian DS, Yang H, Niu SL (2018a) Size-dependent nutrient limitation of tree growth from subtropical to cold temperate forests. Funct Ecol 32:863–875. https://doi.org/10.1111/1365-2435.12975
Li MH, Jiang Y, Wang A, Li XB, Zhu WZ, Yan CF, Du Z, Shi Z, Lei JP, Schönbeck L, He P, Yu FH, Wang X (2018b) Active summer carbon storage for winter persistence in trees at the cold alpine treeline. Tree Physiol 38:1345–1355. https://doi.org/10.1093/treephys/tpy020
Liu JF, Arend M, Yang WJ, Schaub M, Ni YY, Gessler A, Jiang ZP, Rigling A, Li MH (2017) Effects of drought on leaf carbon source and growth of European beech are modulated by soil type. Sci Rep 7:42462. https://doi.org/10.1038/srep42462
Liu MH, Chen SX, Korpelainen H, Zhang H, Wang JR, Huang HH, Yi LT (2021a) Nitrogen addition affects eco-physiological interactions between two tree species dominating in subtropical forests. Plant Physiol Biochem 162:150–160. https://doi.org/10.1016/j.plaphy.2021.02.029
Liu Y, Zhang GH, Luo XZ, Hou EQ, Zheng MH, Zhang LL, He XJ, Shen WJ, Wen DZ (2021b) Mycorrhizal fungi and phosphatase involvement in rhizosphere phosphorus transformations improves plant nutrition during subtropical forest succession. Soil Biol Biochem 153:1–10. https://doi.org/10.1016/j.soilbio.2020.108099
Luo XZ, Hou EQ, Chen JQ, Li J, Zhang LL, Zang XW, Wen DZ (2020) Dynamics of carbon, nitrogen, and phosphorus stocks and stoichiometry resulting from conversion of primary broadleaf forest to plantation and secondary forest in subtropical China. CATENA 193:104606. https://doi.org/10.1016/j.catena.2020.104606
Mariotte P, Cresswell T, Johansen MP, Harrison JJ, Keitel C, Dijkstra FA (2020) Plant uptake of nitrogen and phosphorus among grassland species affected by drought along a soil available phosphorus gradient. Plant Soil 448:121–132. https://doi.org/10.1007/s11104-019-04407-0
McCulloch LA, Porder S (2020) Lower nodule biomass with increased nitrogenase efficiency in Robinia pseudoacacia seedlings when grown under low soil phosphorus conditions. SN Appl Sci 2:1785. https://doi.org/10.1007/s42452-020-03518-z
Mei L, Xiong YM, Gu JC, Wang ZQ, Guo DL (2015) Whole-tree dynamics of non-structural carbohydrate and nitrogen pools across different seasons and in response to girdling in two temperate trees. Oecologia 1177:333–344. https://doi.org/10.1007/s00442-014-3186-1
Ni YY, Jian ZJ, Zeng LX, Liu JF, Lei L, Zhu JH, Xu J, Xiao WF (2022) Climate, soil nutrients, and stand characteristics jointly determine large-scale patterns of biomass growth rates and allocation in Pinus massoniana plantations. For Ecol Manage 504:119839. https://doi.org/10.1016/j.foreco.2021.119839
Osaki M, Shinano T, Tadano T (1991) Redistribution of carbon and nitrogen compounds from the shoot to the harvesting organs during maturation in field crops. Soil Sci Plant Nutr 37:117–128. https://doi.org/10.1080/00380768.1991.10415017
Prietzel J, Falk W, Reger B, Uhl E, Pretzsch H, Zimmermann L (2020) Half a century of Scots pine forest ecosystem monitoring reveals long-term effects of atmospheric deposition and climate change. Glob Change Biol 26:5796–5815. https://doi.org/10.1111/gcb.15265
Richardson AD, Carbone MS, Keenan TF, Czimczlk C, Holling DY, Murakami P, Schaberg PG, Xu XM (2013) Seasonal dynamic and age of stemwood nonstructural carbohydrates in temperate forest trees. New Phytol 197:850–861. https://doi.org/10.1111/nph.12042
Rowland L, da Costa ACL, Galbraith DR, Oliveira RS, Binks OJ, Oliveira AAR, Pullen AM, Doughty CE, Metcalfe DB, Vasconcelos SS, Ferreira LV, Malhi Y, Grace J, Mencuccini M, Meir P (2015) Death from drought in tropical forests is triggered by hydraulics not carbon starvation. Nature 528:119–122. https://doi.org/10.1038/nature15539
Schreeg LA, Santiago LS, Wright SJ, Turner BL (2014) Stem, root, and older leaf N: P ratios are more responsive indicators of soil nutrient availability than new foliage. Ecology 95:2062–2068. https://doi.org/10.1890/13-1671.1
Seifter S, Dayton S, Novic B, Muntwyler E (1950) The estimation of glycogen with the anthrone reagent. Arch Biochem 25:191–200
Signori-Müller C, Oliveira RS, Barros FDV, Tavares JV, Gilpin M, Diniz FC, Zevallos MJM, Yupayccana CAS, Acosta M, Bacca J, Chino RSC, Cuellar GMA, Cumapa ERM, Martinez F, Mullisaca FMP, Nina A, Sanchez JMB, da Silva LF, Tello L, Tintaya JS, Ugarteche MTM, Baker TR, Bittencourt PRL, Borma LS, Brum M, Castro W, Coronado ENH, Cosio EG, Feldpausch TR, Fonseca LDM, Gloor E, Llampazo GF, Malhi Y, Mendoza AM, Moscoso VC, Araujo-Murakami A, Phillips OL, Salinas N, Silveira M, Talbot J, Vasquez R, Mencuccini M, Galbraith D (2021) Non-structural carbohydrates mediate seasonal water stress across Amazon forests. Nat Commun 12:2310. https://doi.org/10.1038/s41467-021-22378-8
Tang ZY, Xu WT, Zhou GY, Bai YF, Li JX, Tang XL, Chen DM, Liu Q, Ma WH, Xiong GM, He HL, He NP, Guo YP, Guo Q, Zhu JL, Han WX, Hu HF, Fang JY, Xie ZQ (2018) Patterns of plant carbon, nitrogen, and phosphorus concentration in relation to productivity in China’s terrestrial ecosystems. Proc Natl Acad Sci U S A 115:4033–4038. https://doi.org/10.1073/pnas.1700295114
Toro L, Pereira-Arias D, Perez-Aviles D, Vargas GG, Soper FM, Gutknecht J, Powers JS (2023) Phosphorus limitation of early growth differs between nitrogen-fixing and nonfixing dry tropical forest tree species. New Phytol 237:766–779. https://doi.org/10.1111/nph.18612
Turner BL, Brenes-Arguedas T, Condit R (2018) Pervasive phosphorus limitation of tree species but not communities in tropical forests. Nature 555:367–370. https://doi.org/10.1038/nature25789
Vance CP, Uhde-Stone C, Allan DL (2003) Phosphorus acquisition and use: critical adaptations by plants for securing a nonrenewable resource. New Phytol 157:423–447. https://doi.org/10.1046/j.1469-8137.2003.00695.x
Wang FC, Chen FS, Wang GG, Mao R, Fang XM, Wang HM, Bu WS (2019) Effects of experimental nitrogen addition on nutrients and nonstructural carbohydrates of dominant understory plants in a Chinese fir plantation. Forests 10:155. https://doi.org/10.3390/f10020155
Way DA, Sage RF (2008) Elevated growth temperatures reduce the carbon gain of black spruce [Picea mariana (Mill.) B.S.P.]. Global Change Biol 14:624–636. https://doi.org/10.1111/j.1365-2486.2007.01513.x
Wright SJ (2022) Low phosphorus levels limit carbon capture by Amazonian forests. Nature 608:476–477. https://doi.org/10.1038/d41586-022-02106-y
Wright SJ, Yavitt JB, Wurzburger N, Turner BL, Tanner EVJ, Sayer E, Santiago LS, Kaspari M, Hedin LO, Harms KE, Garcia MN, Corre MD (2011) Potassium, phosphorus, or nitrogen limit root allocation, tree growth, or litter production in a lowland tropical forest. Ecology 92:1616–1625. https://doi.org/10.1890/10-1558.1
Wright SJ, Turner BL, Yavitt JB, Hams KE, Kaspari M, Tanner EVJ, Bujan J, Griffin EA, Mayor JR, Pasquini SC, Sheldrake M, Garcia MN (2018) Plant responses to fertilization experiments in lowland, species-rich, tropical forests. Ecology 99:1129–1138. https://doi.org/10.1002/ecy.2193
Xiao L, Liu GB, Li P, Xue S (2017) Nitrogen addition has a stronger effect on stoichiometries of non-structural carbohydrates, nitrogen and phosphorus in Bothriochloa ischaemum than elevated CO2. Plant Growth Regul 83:325–334. https://doi.org/10.1007/s10725-017-0298-8
Yu ZP, Wang MH, Huang ZQ, Lin TC, Vadeboncoeur MA, Searle EB, Chen HYH (2018) Temporal changes in soil C-N-P stoichiometry over the past 60 years across subtropical China. Glob Change Biol 24:1308–1320. https://doi.org/10.1111/gcb.13939
Yu L, Song MY, Xia ZC, Korpelainen H, Li CY (2019) Plant-plant interactions and resource dynamics of Abies fabri and Picea brachytyla as affected by phosphorus fertilization. Environ Exp Bot 168:103893. https://doi.org/10.1016/j.envexpbot.2019.103893
Zalamea P, Turner BL, Winter K, Jones FA, Sarmiento C, Dalling JW (2016) Seedling growth responses to phosphorus reflect adult distribution patterns of tropical trees. New Phytol 212:400–408. https://doi.org/10.1111/nph.14045
Zavišić A, Polle A (2018) Dynamics of phosphorus nutrition, allocation and growth of young beech (Fagus sylvatica L.) trees in P-rich and P-poor forest soil. Tree Physiol 38:37–51. https://doi.org/10.1093/treephys/tpx146
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. https://doi.org/10.1038/NPLANTS.2015.50
Zhang D, Jing H, Wang GL (2019) Responses of non-structural carbohydrate content in leaves of different plant species in Pinus tabuliformis plantation to nitrogen addition. Chin J Appl Ecol 30:489–495. https://doi.org/10.13287/j.1001-9332.201902.022
Zhou Y, Watts SE, Boutton TW, Archer SR (2019) Root density distribution and biomass allocation of co-occurring woody plants on contrasting soils in a subtropical savanna parkland. Plant Soil 438:263–279. https://doi.org/10.1007/s11104-019-04018-9
Acknowledgements
We are grateful to the Zigui Forest Ecosystem Research Station for providing the experimental site and experimental supports.
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This work was supported by grants from Chinese Academy of Forestry (grant number: CAFYBB2021QD002).
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Highlights
• Phosphorus promoted the relative growth rate of Pinus massoniana seedlings in a relatively low but fact-based P range.
• Biomass proportion of fine root but not biomass decreased with P addition.
• In low-P condition, C allocation patterns to different organs depended on organs’ synthesis and C utilization patterns.
• NSC existed more in different fractions in needles and fine root in low-P groups.
• Facing P deficiency, P. massoniana seedlings maintained growth by regulating the allocation of C and fractions of NSC.
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Xu, J., Lei, L., Zeng, L. et al. The Responses of C Allocation of New Needle and Fine Root Affected the Phosphorus Adaptation of Pinus massoniana Seedlings. J Soil Sci Plant Nutr 24, 295–307 (2024). https://doi.org/10.1007/s42729-023-01500-3
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DOI: https://doi.org/10.1007/s42729-023-01500-3