Abstract
Key message
Trees adjust their root morphological characteristics to respond heterogeneous phosphorus conditions, and root length and root-to-shoot ratio will increase to improve phosphorus nutrient absorption in heterogeneous phosphorus soils.
Abstract
This study examined the responses of root morphology and seedling growth to homogeneous and heterogeneous phosphorus (P) supplies in three major tree species (Cunninghamia lanceolata, Pinus massoniana, and Phoebe zhennan) in southern China. Pot experiments including two homo-P and five hetero-P supplies with different P dosage levels were conducted across three species. Root length, root average diameter, root biomass, aboveground biomass, root-to-shoot ratio, P accumulation, P-efficiency ratio, and increments in height and diameter of seedlings were quantified. Roots of the three species showed symmetric and asymmetric growth in response to homo-P and hetero-P supplies, respectively. The root biomass and average diameter were greater in the P-rich patch than in the P-poor patch, and roots in the P-poor patch were thinner and longer than their opposite counterparts. The root length and biomass were higher in hetero-P treatments than in homo-P treatments at an equivalent P dosage. The heterogeneity magnitude was negatively correlated with the aboveground biomass and positively correlated with the root biomass and root-to-shoot ratio. The P-efficiency ratio was negatively correlated with the dose of added P. The growth responses include a comprehensive adjustment in the root morphology and root-to-shoot ratio. The root growth pattern can change to adapt to lower P availability in soil, and the root-to-shoot ratio will increase to optimize nutrient partitioning and improve P-nutrient absorption in hetero-P soils.
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References
Arnon DI (1938) Microelements in culture-solution experiments with higher plants. Am J Bot 25:322–325. https://doi.org/10.1002/j.1537-2197.1938.tb09223.x
Baligar VC, Fageria NK (2015) Nutrient use efficiency in plants: an overview. Springer, New Delhi
Bates TR, Lynch JP (2001) Root hairs confer a competitive advantage under low phosphorus availability. Plant Soil 236:243–250. https://doi.org/10.1023/A:1012791706800
Beebe SE, Rojas-Pierce M, Yan X, Blair MW, Pedraza F, Muñoz F, Tohme J, Lynch JP (2006) Quantitative trait loci for root architecture traits correlated with phosphorus acquisition in common bean. Crop Sci 46:413–423. https://doi.org/10.2135/cropsci2005.0226
Blair BC, Perfecto I (2004) Successional status and root foraging for phosphorus in seven tropical tree species. Can J For Res 34:1128–1135. https://doi.org/10.1139/x04-004
Cahn MD, Zobel RW, Bouldin DR (1989) Relationship between root elongation rate and diameter and duration of growth of lateral roots of maize. Plant Soil 119:271–279. https://doi.org/10.1007/BF02370419
Chen H (2003) Phosphatase activity and P fractions in soils of an 18-year-old Chinese fir (Cunninghamia lanceolata) plantation. For Ecol Manag 178:301–310. https://doi.org/10.1016/s0378-1127(02)00478-4
Chen YL, Dunbabin VM, Postma JA, Diggle AJ, Siddique KHM, Rengel Z (2013) Modelling root plasticity and response of narrow-leafed lupin to heterogeneous phosphorus supply. Plant Soil 372:319–337. https://doi.org/10.1007/s11104-013-1741-x
Comas LH, Callahan HS, Midford PE (2014) Patterns in root traits of woody species hosting arbuscular and ectomycorrhizas: implications for the evolution of belowground strategies. Ecol Evol 4:2979–2990. https://doi.org/10.1002/ece3.1147
Crick JC, Grime JP (1987) Morphological plasticity and mineral nutrient capture in two herbaceous species of contrasted ecology. New Phytol 107:403–414. https://doi.org/10.1111/j.1469-8137.1987.tb00192.x
Dakora FD, Phillips DA (2002) Root exudates as mediators of mineral acquisition in low-nutrient environments. Plant Soil 245:35–47. https://doi.org/10.1023/A%3A1020809400075
Du J, Lu CT (2009) Study on growth regularity of Phoebe zhennan plantation. J Zhejiang For Sci Technol 29:9–12
Einsmann JC, Jones RH, Pu M, Mitchell RJ (1999) Nutrient foraging traits in 10 co-occurring plant species of contrasting life forms. J Ecol 87:609–619
Farley RA, Fitter AH (1999) The responses of seven co-occurring woodland herbaceous perennials to localized nutrient-rich patches. J Ecol 87:849–859. https://doi.org/10.1046/j.1365-2745.1999.00396.x
Fita A, Nuez F, Picó B (2011) Diversity in root architecture and response to P deficiency in seedlings of Cucumis melo L. Euphytica 181:323–339. https://doi.org/10.1007/s10681-011-0432-z
Fransen B, Kroon HD, Berendse F (1998) Root morphological plasticity and nutrient acquisition of perennial grass species from habitats of different nutrient availability. Oecologia 115:351. https://doi.org/10.1007/s004420050527
Fransen B, Blijjenberg J, Kroon HD (1999) Root morphological and physiological plasticity of perennial grass species and the exploitation of spatial and temporal heterogeneous nutrient patches. Plant Soil 211:179–189. https://doi.org/10.1023/A%3A1004684701993
Gao J, Zhang W, Li J, Long H, He W, Li X (2016) Amplified fragment length polymorphism analysis of the population structure and genetic diversity of Phoebe zhennan (Lauraceae), a native species to China. Biochem Syst Ecol 64:149–155. https://doi.org/10.1016/j.bse.2015.11.001
Gourley CJP, Allan DL, Russelle MP (1994) Plant nutrient efficiency: a comparison of definitions and suggested improvement. Plant Soil 158:29–37. https://doi.org/10.1007/BF00007914
Gruber BD, Giehl RF, Friedel S, Von WN (2013) Plasticity of the arabidopsis root system under nutrient deficiencies. Plant Physiol 163:161–179. https://doi.org/10.1104/pp.113.218453
Guo D, Xia M, Wei X, Chang W, Liu Y, Wang Z (2008) Anatomical traits associated with absorption and mycorrhizal colonization are linked to root branch order in twenty-three Chinese temperate tree species. New Phytol 180:673–683. https://doi.org/10.1111/j.1469-8137.2008.02573.x
Hammond JP, White PJ (2008) Sucrose transport in the phloem: integrating root responses to phosphorus starvation. J Exp Bot 59:93–109. https://doi.org/10.1093/jxb/erm221
He Y, Liao H, Yan X (2003) Localized supply of phosphorus induces root morphological and architectural changes of rice in split and stratified soil cultures. Plant Soil 248:247–256. https://doi.org/10.1023/A%3A1022351203545
Henry A, Kleinman PJA, Lynch JP (2009) Phosphorus runoff from a phosphorus deficient soil under common bean (Phaseolus vulgaris L.) and soybean (Glycine max L.) genotypes with contrasting root architecture. Plant Soil 317:1–16. https://doi.org/10.1007/s11104-008-9784-0
Hodge A (2004) The plastic plant: root responses to heterogeneous supplies of nutrients. New Phytol 162:9–24. https://doi.org/10.1111/j.1469-8137.2004.01015.x
Hodge A, Stewart J, Robinson D, Griffiths BS, Fitter AH (1998) Root proliferation, soil fauna and plant nitrogen capture from nutrient-rich patches in soil. New Phytol 139:479–494. https://doi.org/10.1046/j.1469-8137.1998.00216.x
Hu YF, Ye XS, Lei S, Duan HY, Xu FS (2010) Genotypic differences in root morphology and phosphorus uptake kinetics in Brassica napus under low phosphorus supply. J Plant Nutr 33:889–901. https://doi.org/10.1080/01904161003658239
Jackson RB, Caldwell MM (1993) The scale of nutrient heterogeneity around individual plants and its quantification with geostatistics. Ecology 74:612–614. https://doi.org/10.2307/1939320
Lambers H, Shane MW, Cramer MD, Pearse SJ, Veneklaas EJ (2006) Root structure and functioning for efficient acquisition of phosphorus: matching morphological and physiological traits. Ann Bot 98:693–713. https://doi.org/10.1093/aob/mcl114
Lambers H, Martinoia E, Renton M (2015) Plant adaptations to severely phosphorus-impoverished soils. Curr Opin Plant Biol 25:23–31. https://doi.org/10.1016/j.pbi.2015.04.002
Li J, Xie Y, Dai A, Liu L, Li Z (2009) Root and shoot traits responses to phosphorus deficiency and QTL analysis at seedling stage using introgression lines of rice. J Genet Genom 36:173–183. https://doi.org/10.1016/S1673-8527(08)60104-6
Li L, Mccormack ML, Chen F, Wang H, Ma Z, Guo D (2019) Different responses of absorptive roots and arbuscular mycorrhizal fungi to fertilization provide diverse nutrient acquisition strategies in Chinese fir. For Ecol Manag 433:64–72. https://doi.org/10.1016/j.foreco.2018.10.055
Liang X, Liu AQ, Ma XQ, Feng LZ, Huang YJ (2006) Comparison of the phosphorus characteristics of different Chinese fir clones. Chin J Plant Ecol 30:1005–1011
Liao H, Yan XL, Rubio G, Beebe SE, Blair MW, Lynch JP (2004) Genetic mapping of basal root gravitropism and phosphorus acquisition efficiency in common bean. Funct Plant Biol 31:959. https://doi.org/10.1071/FP03255
Liu B, Liu Q, Daryanto S, Guo S, Huang Z, Wang Z, Wang L, Ma X (2018) Responses of Chinese fir and Schima superba seedlings to light gradients: implications for the restoration of mixed broadleaf-conifer forests from Chinese fir monocultures. For Ecol Manag 419–420:51–57. https://doi.org/10.1016/j.foreco.2018.03.033
Long HL (2011) An analysis of the growth of Phoebe zhennan in Sichuan. J Sichuan For Sci Technol 32:89–91
Lynch JP (2011) Root phenes for enhanced soil exploration and phosphorus acquisition: tools for future crops. Plant Physiol 156:1041–1049. https://doi.org/10.1104/pp.111.175414
Ma Q, Rengel Z, Siddique KHM (2011) Wheat and white lupin differ in root proliferation and phosphorus use efficiency under heterogeneous soil P supply. Crop Pasture Sci 62:467. https://doi.org/10.1071/cp10386
Miller CR, Ochoa I, Nielsen KL, Beck D, Lynch JP (2003) Genetic variation for adventitious rooting in response to low phosphorus availability: potential utility for phosphorus acquisition from stratified soils. Funct Plant Biol 30:973–985. https://doi.org/10.1071/FP03078
Nguyen TN, Nakabayashi K, Mohapatra PK, Thompson J, Fujita K (2003) Effect of nitrogen deficiency on biomass production, photosynthesis, carbon partitioning, and nitrogen nutrition status of Melaleuca and Eucalyptus species. Soil Sci Plant Nutr 49:99–109. https://doi.org/10.1080/00380768.2003.10409985
Péret B, Desnos T, Jost R, Kanno S, Berkowitz O, Nussaume L (2014) Root architecture responses: in search of phosphate. Plant Physiol 166:1713–1723. https://doi.org/10.1104/pp.114.244541
Puig J, Pauluzzi G, Guiderdoni E, Gantet P (2012) Regulation of shoot and root development through mutual signaling. Mol Plant 5:974–983. https://doi.org/10.1093/mp/sss047
Richardson AE, Lynch JP, Ryan PR, Delhaize E, Smith FA, Smith SE, Harvey PR, Ryan MH, Veneklaas EJ, Lambers H, Oberson A, Culvenor RA, Simpson RJ (2011) Plant and microbial strategies to improve the phosphorus efficiency of agriculture. Plant Soil 349:121–156. https://doi.org/10.1007/s11104-011-0950-4
Robinson D, Rorison IH (1983) A comparison of the responses of Lolium perenne L. Holcus lanatus L. and Deschampsia flexuosa (L.) trin. to a localized supply of nitrogen. New Phytol 94:263–273. https://doi.org/10.1111/j.1469-8137.1983.tb04499.x
Rothstein DE, Zak DR, Pregitzer KS, Curtis PS (2000) Kinetics of nitrogen uptake by Populus tremuloides in relation to atmospheric CO2 and soil nitrogen availability. Tree Physiol 20:265–270. https://doi.org/10.1093/treephys/20.4.265
Scherer H, Sharma S (2002) Phosphorus fractions and phosphorus delivery potential of a luvisol derived from loess amended with organic materials. Biol Fertil Soils 35:414–419. https://doi.org/10.1007/s00374-002-0488-y
Schweiger PF, Robson AD, Barrow NJ, Abbott LK (2007) Arbuscular mycorrhizal fungi from three genera induce two-phase plant growth responses on a high P-fixing soil. Plant Soil 292:181–192. https://doi.org/10.1007/s11104-007-9214-8
Suriyagoda LDB, Ryan MH, Renton M, Lambers H (2011) Above- and below-ground interactions of grass and pasture legume species when grown together under drought and low phosphorus availability. Plant Soil 348:281–297. https://doi.org/10.1007/s11104-011-0754-6
Tariq A, Pan K, Olatunji OA, Graciano C, Li Z, Sun F, Sun X, Song D, Chen W, Zhang A, Wu X, Zhang L, Mingrui D, Xiong Q, Liu C (2017) Phosphorous application improves drought tolerance of Phoebe zhennan. Front Plant Sci 8:1561. https://doi.org/10.3389/fpls.2017.01561
Vance CP, Uhdestone 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 X, Pan Q, Chen F, Yan X, Liao H (2011) Effects of co-inoculation with arbuscular mycorrhizal fungi and rhizobia on soybean growth as related to root architecture and availability of N and P. Mycorrhiza 21:173–181. https://doi.org/10.1007/s00572-010-0319-1
Wang Q, Li YG, Liu XH, Wu DK, Liu FQ, He YH (2013) Community composition and structure of Phoebe zhennan forest in Enshi, Hubei Province. For Res 26:21–28
Wu P, Ma X, Tigabu M, Wang C, Liu A, Odén PC (2011) Root morphological plasticity and biomass production of two Chinese fir clones with high phosphorus efficiency under low phosphorus stress. Can J For Res 41:228–234. https://doi.org/10.1139/x10-198
Zhang Y, Zhou Z, Yang Q (2013) Genetic variations in root morphology and phosphorus efficiency of Pinus massoniana under heterogeneous and homogeneous low phosphorus conditions. Plant Soil 364:93–104. https://doi.org/10.1007/s11104-012-1352-y
Zhou C, Jiang W, Li Y, Hou X, Liu A, Cai L (2016) Morphological plasticity and phosphorus uptake mechanisms of hybrid Eucalyptus roots under spatially heterogeneous phosphorus stress. J For Res 28:713–724. https://doi.org/10.1007/s11676-016-0335-x
Zobel RW, Alloush GA, Belesky DP (2006) Differential root morphology response to no versus high phosphorus, in three hydroponically grown forage chicory cultivars. Environ Exp Bot 57:201–208. https://doi.org/10.1016/j.envexpbot.2005.05.002
Zou X, Wu P, Chen N, Wang P, Ma X (2015) Chinese fir root response to spatial and temporal heterogeneity of phosphorus availability in the soil. Can J For Res 45:402–410. https://doi.org/10.1139/cjfr-2014-0384
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This research was jointly supported by the National Natural Science Foundation of China (31700557 and 31870614) and the Science and Technology Major Project of Fujian Province, China (2018NZ0001-1).
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Yan, XL., Wang, C., Ma, X. et al. Root morphology and seedling growth of three tree species in southern China in response to homogeneous and heterogeneous phosphorus supplies. Trees 33, 1283–1297 (2019). https://doi.org/10.1007/s00468-019-01858-x
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DOI: https://doi.org/10.1007/s00468-019-01858-x