Preference for Insoluble Phosphorus Forms and Adaptation Mechanisms in Pinus sibirica Seedlings

doi:10.7525/j.issn.1673-5102.2026.03.015

Abstract

Abstract:

Phosphorus（P） predominantly exists in forest soils as insoluble forms（such as inorganic and organic phosphorus）， and its low availability is a major factor limiting tree growth. Pinus sibirica， a key constructive species of the cold-temperate coniferous forest， faces challenges when its seedlings are transplanted to the acidic soils of the Greater Khingan Mountains， where insufficient available phosphorus adversely affects seedling survival and growth. To explore the adaptation mechanisms of P. sibirica to insoluble P， a pot experiment was conducted using 2-year-old seedlings as test material. Treatments included a control（no P addition） and three P addition levels-50% （17.40 mg⋅kg^-1）， 100% （34.80 mg⋅kg^-1）， and 200% （69.60 mg⋅kg^-1）-applied via four different P sources： calcium phytate， lecithin， aluminum phosphate， and iron phosphate. Seedling responses in biomass allocation， root morphology， and whole-plant phosphorus use efficiency（PUE） were analyzed. The results showed that：（1）Different P sources significantly affected seedling growth（P<0.05）. The iron phosphate treatment -particularly at 200% P addition level-significantly promoted biomass accumulation in all organs and total seedling biomass， whereas organic P sources（calcium phytate and lecithin） had no significant promoting effects. （2）PUE was significantly influenced by the interaction between P source type and level（P<0.05）. The highest PUE occurred under the 50% iron phosphate-addition level and declined with increasing levels； in contrast， PUE remained low and showed no significant trend under organic P source treatments. （3）Root morphology exhibited plasticity in response to insoluble P stress. Compared with the control， all P application treatments increased the specific root length and specific surface area of first-order roots but reduced their tissue density. Low-level iron phosphate induced a resource-acquisition strategy（characterized by high specific root length and low tissue density）， whereas a conservative strategy predominated at high P-addition levels. （4）A comprehensive evaluation indicated that the 200% iron phosphate treatment achieved the highest composite score， followed by 200% aluminum phosphate- and 100% lecithin-addition level， indicating that inorganic P sources-especially iron phosphate-are more conducive to P. sibirica seedling growth. In conclusion， P. sibirica enhanced its phosphorus acquisition capacity by modulating root morphological traits， adjusting biomass allocation patterns， and optimizing PUE， with iron phosphate being the dominant P form efficiently utilized by this species. In future afforestation and tending practices， iron phosphate is recommended as the preferred phosphorus fertilizer for P. sibirica seedlings， and fertilization strategies should adhere to the principle of “low concentration for root development promotion and high concentration for aboveground growth promotion”. This study provides scientific guidance for improving seedling quality and afforestation survival rates of P. sibirica in acidic soil regions.

Key words: Pinus sibirica, insoluble phosphorus sources, phosphorus utilization efficiency, root morphology, biomass allocation

CLC Number:

S714.8

Yali YIN, Lixue YANG, Junyi YU, Juntong CHEN, Hui DONG, Huifeng LIU, Di XU. Preference for Insoluble Phosphorus Forms and Adaptation Mechanisms in Pinus sibirica Seedlings[J]. Bulletin of Botanical Research, 2026, 46(3): 557-569.

Figures/Tables 8

Table 1

Table 2

Table 3

Table 4

Fig.1

Fig.2

Fig.3

Table 5

References 42

[1]	郭艳，陈后英，铁烈华，等.外生菌根真菌橙黄硬皮马勃对不同难溶性磷酸盐供应水平下马尾松幼苗生长及生理特性的影响［J］.应用与环境生物学报，2025，31（1）：87-95.
	GUO Y， CHEN H Y， TIE L H，et al.Effects of the ectomycorrhizal fungi Scleroderma citrinum on the growth and physiological characteristics of Pinus massoniana seedlings under different insoluble phosphate supply levels［J］.Chinese Journal of Applied and Environmental Biology，2025，31（1）：87-95.
[2]	PRABHU N， BORKAR S， GARG S.Phosphate solubilization by microorganisms［M］//MEENA S N， NAIK M M. Advances in biological science research：a practical approach.Amsterdam：Academic Press，2019：161-176.
[3]	BAI K H， WANG W Y， ZHANG J N，et al.Effects of phosphorus-solubilizing bacteria and biochar application on phosphorus availability and tomato growth under phosphorus stress［J］.BMC Biology，2024，22（1）：211.
[4]	AMADOU I， FAUCON M P， HOUBEN D.Role of soil minerals on organic phosphorus availability and phosphorus uptake by plants［J］.Geoderma，2022，428：116125.
[5]	DARCH T， BLACKWELL M S A， HAWKINS J M B，et al.A meta-analysis of organic and inorganic phosphorus in organic fertilizers，soils，and water：implications for water quality［J］.Critical Reviews in Environmental Science and Technology，2014，44（19）：2172-2202.
[6]	江盈，邹锋，黄建，等.六个外生菌根真菌菌株在不同难溶性磷源下的溶磷特性［J］.菌物学报，2023，42（6）：1311-1329.
	JIANG Y， ZOU F， HUANG J，et al.Phosphorus dissolving characteristics of six ectomycorrhizal fungal strains under different insoluble phosphorus sources［J］.Mycosystema，2023，42（6）：1311-1329.
[7]	郭旋，胡中民，李胜功，等.氮磷添加对内蒙古温带典型草原地下生物量的影响［J］.生态学杂志，2021，40（4）：929-939.
	GUO X， HU Z M， LI S G，et al.Effects of nitrogen and phosphorus additions on belowground biomass of temperate typical steppe in Inner Mongolia［J］.Chinese Journal of Ecology，2021，40（4）：929-939.
[8]	ZHANG K， ZHENG D F， GU Y，et al.Utilizing soil organic phosphorus for sustainable crop production：insights into the rhizosphere［J］.Plant and Soil，2024，498（1）：57-75.
[9]	MA Z Q， GUO D L， XU X L，et al.Evolutionary history resolves global organization of root functional traits［J］.Nature，2018，555（7694）：94-97.
[10]	LAMBERS H， SHANE M W， CRAMER M D，et al.Root structure and functioning for efficient acquisition of phosphorus：matching morphological and physiological traits［J］.Annals of Botany，2006，98（4）：693-713.
[11]	蔡智，王庆成，张勇，等.遮阴和磷限制下胡桃楸1级根养分吸收策略选择［J］.应用生态学报，2023，34（12）：3239-3244.
	CAI Z， WANG Q C， ZHANG Y，et al.Nutrient uptake strategy selection by first-order roots of Juglans mandshurica under shading and phosphorus limitation［J］.Chinese Journal of Applied Ecology，2023，34（12）：3239-3244.
[12]	NIU Y F， CHAI R S， JIN G L，et al.Responses of root architecture development to low phosphorus availability：a review［J］.Annals of Botany，2013，112（2）：391-408.
[13]	白虓宇，李秀芳，李传飞，等.磷高效水稻材料的根系形态结构特征［J］.植物营养与肥料学报，2024，30（5）：1032-1042.
	BAI X Y， LI X F， LI C F，et al.The root morphological and structural characteristics of phosphorus-efficient rice materials［J］.Plant Nutrition and Fertilizer Science，2024，30（5）：1032-1042.
[14]	韦如萍，胡德活，陈金慧，等.低磷胁迫下杉木无性系根系形态及养分利用响应研究［J］.南京林业大学学报（自然科学版），2018，42（2）：1-8.
	WEI R P， HU D H， CHEN J H，et al.Response of roots morphological characteristics and nutrient utilization to low phosphorus stress among five clones of Cunninghamia lanceolata（Lamb.） Hook.［J］.Journal of Nanjing Forestry University （Natural Sciences Edition），2018，42（2）：1-8.
[15]	胡梦婷，罗旭.大兴安岭林区引种西伯利亚红松研究进展［J］.生态科学，2022，41（3）：237-244.
	HU M T， LUO X.Research progress of introduced Pinus sibirica in Great Xing’an Mountains［J］.Ecological Science，2022，41（3）：237-244.
[16]	刘会锋，孙璐，张杰，等.加格达奇区西伯利亚红松种源和单株遗传变异及选择［J］.东北林业大学学报，2025，53（9）：70-74.
	LIU H F， SUN L， ZHANG J，et al.Genetic variation and selection of provenances and individual trees of Pinus sibirica in Jiagedaqi District［J］.Journal of Northeast Forestry University，2025，53（9）：70-74.
[17]	刘桂丰，杨传平，赵光仪.珍贵树种西伯利亚红松引进的可行性［J］.应用生态学报，2002，13（11）：1483-1486.
	LIU G F， YANG C P， ZHAO G Y.Feasibility to introduce rare tree species Pinus sibirica into China［J］.Chinese Journal of Applied Ecology，2002，13（11）：1483-1486.
[18]	韩智明，辛颖，赵雨森.大兴安岭火烧迹地植被恢复过程土壤解磷微生物种群及活性［J］.东北林业大学学报，2020，48（8）：55-60.
	HAN Z M， XIN Y， ZHAO Y S.Soil phosphate-dissolving microorganisms in the process of vegetation restoration in burned area of Daxing’an Mountains［J］.Journal of Northeast Forestry University，2020，48（8）：55-60.
[19]	陈晨，杨雨春，申方圆，等.间伐对红松吸收根功能性状的影响［J］.生态学报，2025，45（8）：3969-3977.
	CHEN C， YANG Y C， SHEN F Y，et al.Effects of thinning on absorptive root functional traits of Pinus koraiensis ［J］.Acta Ecologica Sinica，2025，45（8）：3969-3977.
[20]	吴文景，梅辉坚，许静静，等.供磷水平及方式对杉木幼苗根系生长和磷利用效率的影响［J］.生态学报，2020，40（6）：2010-2018.
	WU W J， MEI H J， XU J J，et al.Effects of phosphorus supply levels and methods on root growth and phosphorus use efficiency of Chinese fir seedling［J］.Acta Ecologica Sinica，2020，40（6）：2010-2018.
[21]	LÓPEZ-ARREDONDO D L， LEYVA-GONZÁLEZ M A， GONZÁLEZ-MORALES S I，et al.Phosphate nutrition：improving low-phosphate tolerance in crops［J］.Annual Review of Plant Biology，2014，65：95-123.
[22]	章爱群，贺立源，赵会娥，等.有机酸对不同磷源条件下土壤无机磷形态的影响［J］.应用与环境生物学报，2009，15（4）：474-478.
	ZHANG A Q， HE L Y， ZHAO H E，et al.Effect of organic acids on inorganic phosphorus transformation in soil with different phosphorus sources［J］.Chinese Journal of Applied and Environmental Biology，2009，15（4）：474-478.
[23]	NAWAZ M， SUN J F， SHABBIR S，et al.A review of plants strategies to resist biotic and abiotic environmental stressors［J］.Science of the Total Environment，2023，900：165832.
[24]	VAISHLYA O， KARBYSHEVA K， SARSEKOVA D，et al.Ecological aspects of Pinus sibirica du tour mycotrophy in forest ecosystems of west Siberia［J］.IOP Conference Series：Earth and Environmental Science，2019，224：012049.
[25]	ROSLING A， MIDGLEY M G， CHEEKE T，et al.Phosphorus cycling in deciduous forest soil differs between stands dominated by ecto- and arbuscular mycorrhizal trees［J］.New Phytologist，2016，209（3）：1184-1195.
[26]	VAN HEES P A W， VINOGRADOFF S I， EDWARDS A C，et al.Low molecular weight organic acid adsorption in forest soils：effects on soil solution concentrations and biodegradation rates［J］.Soil Biology and Biochemistry，2003，35（8）：1015-1026.
[27]	D’AMICO M， ALMEIDA J P， BARBIERI S，et al.Ectomycorrhizal utilization of different phosphorus sources in a glacier forefront in the Italian Alps［J］.Plant and Soil，2020，446（1）：81-95.
[28]	NEHLS U， PLASSARD C.Nitrogen and phosphate metabolism in ectomycorrhizas［J］.New Phytologist，2018，220（4）：1047-1058.
[29]	杨杰文，钟来元，郭荣发，等.有机酸对砖红壤的溶解及固定态磷素的活化［J］.环境化学，2010，29（6）：1063-1067.
	YANG J W， ZHONG L Y， GUO R F，et al.Dissolution of latosol and the release of immobilized phosphorus promoted by organic acids［J］.Environmental Chemistry，2010，29（6）：1063-1067.
[30]	崔福星，宋金凤，杨迪.养分缺乏下外源有机酸对暗棕壤磷有效性及落叶松幼苗吸收积累磷的影响［J］.水土保持学报，2012，26（6）：116-121.
	CUI F X， SONG J F， YANG D.Effects of exogenous organic acids on P availability of dark brown forest soils and P absorption and accumulation in Larix olgensis seedlings with nutrient deficiency［J］.Journal of Soil and Water Conservation，2012，26（6）：116-121.
[31]	CHEN Q C， HU T， LI X H，et al.Phosphorylation of SWEET sucrose transporters regulates plant root：shoot ratio under drought［J］.Nature Plants，2022，8（1）：68-77.
[32]	解亚鑫，许涵，陈洁，等.不同氮磷添加浓度对豆科3种树木幼苗生长及生物量分配的影响［J］.植物科学学报，2019，37（5）：662-671.
	XIE Y X， XU H， CHEN J，et al.Effects of varied soil nitrogen and phosphorus concentrations on the growth and biomass allocation of three leguminous tree seedlings［J］.Plant Science Journal，2019，37（5）：662-671.
[33]	LINKOHR B I， WILLIAMSON L C， FITTER A H，et al.Nitrate and phosphate availability and distribution have different effects on root system architecture of Arabidopsis ［J］.The Plant Journal，2002，29（6）：751-760.
[34]	REWALD B， RAVEH E， GENDLER T，et al.Phenotypic plasticity and water flux rates of Citrus root orders under salinity［J］.Journal of Experimental Botany，2012，63（7）：2717-2727.
[35]	LIU R Q， HUANG Z Q， LUKE MCCORMACK M，et al.Plasticity of fine-root functional traits in the litter layer in response to nitrogen addition in a subtropical forest plantation［J］.Plant and Soil，2017，415（1）：317-330.
[36]	黄玉林.苔草属植物胡萝卜状根对难溶性磷源响应及地上生物量调控机制研究［D］.杨凌：西北农林科技大学，2024.
	HUANG Y L.Response of duaciform roots to insoluble phosphorus sources and the mechanism of aboveground biomass regulation in Carex ［D］.Yangling：Northwest A & F University，2024.
[37]	ZHOU C W， CUI W J， YUAN T，et al.Root foraging behavior of two agronomical herbs subjected to heterogeneous P pattern and high Ca stress［J］.Agronomy，2022，12（3）：624.
[38]	孙佳慧，史海兰，陈科宇，等.植物细根功能性状的权衡关系研究进展［J］.植物生态学报，2023，47（8）：1055-1070.
	SUN J H， SHI H L， CHEN K Y，et al.Research advances on trade-off relationships of plant fine root functional traits［J］.Chinese Journal of Plant Ecology，2023，47（8）：1055-1070.
[39]	杜旭，黄平升，杨梅.不同磷肥对尾巨桉DH3229苗木生长及抗性生理的影响［J］.森林与环境学报，2020，40（5）：526-533.
	DU X， HUANG P S， YANG M.Phosphorus fertilizers on the growth and resistance physiology of Eucalyptus urophylla × Eucalyptus grandis DH3229 seedlings［J］.Journal of Forest and Environment，2020，40（5）：526-533.
[40]	袁军，谭晓风，叶思诚，等.不同磷源对酸性红壤养分及油茶幼苗生长的影响［J］.西北农林科技大学学报（自然科学版），2013，41（4）：155-160.
	YUAN J， TAN X F， YE S C，et al.Effects of phosphates from different sources on the growth of Camellia oleifera seedlings and content of nutrients in acidic soil［J］.Journal of Northwest A&F University （Natural Science Edition），2013，41（4）：155-160.
[41]	董利虎，李凤日，贾炜玮.林木竞争对红松人工林立木生物量影响及模型研究［J］.北京林业大学学报，2013，35（6）：15-22.
	DONG L H， LI F R， JIA W W.Effects of tree competition on biomass and biomass models of Pinus koraiensis plantation［J］.Journal of Beijing Forestry University，2013，35（6）：15-22.
[42]	BUEIS T， BRAVO F， PANDO V，et al.Phosphorus availability in relation to soil properties and forest productivity in Pinus sylvestris L.plantations［J］.Annals of Forest Science，2019，76（4）：97.

磷源 Phosphate source	分子式 Molecular formula	相对分子质量 Relative molecular mass	磷质量分数 P mass fraction/%
植酸钙 Calcium phytate	C₆H₆Ca₆O₂₄P₆	888.36	20.92
卵磷脂 Lecithin	C₄₂H₈₀NO₈P	734.07	4.22
磷酸铝 Aluminum phosphate	AlPO₄	121.95	25.40
磷酸铁 Iron（Ⅲ） phosphate	FePO₄	150.82	20.53

处理 Treatment	水平 Level	磷元素添加水平 P addition level/（mg·kg^-1）	化合物添加量 Compound application amount/g
CK	0	0	0
T1	50%	17.4	0.742 2
T2	100%	34.8	1.484 4
T3	200%	69.6	2.968 8
T4	50%	17.4	0.149 7
T5	100%	34.8	0.299 4
T6	200%	69.6	0.598 8
T7	50%	17.4	0.123 3
T8	100%	34.8	0.246 6
T9	200%	69.6	0.493 2
T10	50%	17.4	0.152 6
T11	100%	34.8	0.305 2
T12	200%	69.6	0.610 4

处理 Treatment	施磷水平 P addition level	叶生物量 Leaf biomass/g	茎生物量 Stem biomass/g	根生物量 Root biomass/g	地上生物量 Aboveground biomass/g	总生物量 Total biomass/g	根冠比 Root-shoot ratio
CK	0	0.18±0.06^a	0.38±0.05^bc	0.28±0.06^abc	0.56±0.11^abc	0.85±0.17^bcd	0.50±0.01^ab
卵磷脂	50%	0.24±0.07^a	0.39±0.04^abc	0.27±0.01^abc	0.64±0.09^abc	0.90±0.08^abcd	0.43±0.06^ab
	100%	0.27±0.08^a	0.38±0.03^bc	0.37±0.07^a	0.65±0.10^abc	1.02±0.11^abc	0.59±0.15^a
	200%	0.39±0.25^a	0.37±0.03^bc	0.27±0.04^abc	0.76±0.26^abc	1.03±0.29^abc	0.41±0.09^ab
植酸钙	50%	0.26±0.05^a	0.42±0.02^abc	0.28±0.01^abc	0.68±0.04^abc	0.96±0.03^abcd	0.42±0.04^ab
	100%	0.19±0.01^a	0.39±0.02^abc	0.18±0.01^c	0.59±0.02^abc	0.76±0.01^cd	0.30±0.02^b
	200%	0.24±0.00^a	0.37±0.02^bc	0.21±0.00^bc	0.61±0.02^abc	0.82±0.02^bcd	0.35±0.07^ab
磷酸铝	50%	0.16±0.01^a	0.36±0.01^bc	0.22±0.01^bc	0.52±0.01^bc	0.74±0.01^cd	0.41±0.00^ab
	100%	0.33±0.11^a	0.42±0.05^abc	0.34±0.05^a	0.75±0.09^abc	1.09±0.05^abc	0.49±0.12^ab
	200%	0.39±0.05^a	0.49±0.04^ab	0.32±0.03^ab	0.88±0.10^ab	1.19±0.12^ab	0.36±0.03^ab
磷酸铁	50%	0.16±0.02^a	0.28±0.36^c	0.17±0.03^c	0.44±0.01^c	0.61±0.04^d	0.37±0.07^ab
	100%	0.24±0.04^a	0.36±0.03^bc	0.28±0.03^abc	0.60±0.06^abc	0.87±0.08^bcd	0.47±0.06^ab
	200%	0.39±0.10^a	0.53±0.11^a	0.38±0.04^a	0.92±0.16^a	1.30±0.18^a	0.43±0.06^ab

变异来源 Source of variation	自由度 d_f	F
变异来源 Source of variation	自由度 d_f	磷利用效率 Total plant P use efficiency	根系磷含量 Root P content	茎磷含量 Stem P content	叶磷含量 Leaf P content
难溶性磷类型 The type	3	1.737^**	3.904^*	0.422	0.763
施磷水平 P addition level	2	0.469^**	2.547	6.313^**	0.131
难溶性磷类型×施磷水平 The type×P addition level	6	1.230^**	4.605^**	0.290	0.057

处理 Treatment	施磷水平 P addition level	第1主成分 Component 1	第2主成分 Component 2	第3主成分 Component 3	综合得分 Comprehensive component score	排名 Rank
T12	200%	2.05	0.53	-0.41	1.01	1
T9	200%	1.64	-0.16	-1.07	0.46	2
T2	100%	-0.30	0.31	2.12	0.45	3
T8	100%	0.50	-0.10	0.79	0.39	4
T3	200%	0.44	-0.03	0.43	0.29	5
CK	0	-0.93	2.73	-0.75	0.23	6
T4	50%	0.21	-0.90	1.04	0.07	7
T11	100%	-0.63	0.89	0.21	0.03	8
T1	50%	-0.18	-0.26	0.75	0.02	9
T6	200%	-0.16	-0.62	-0.68	-0.42	10
T5	100%	-0.20	-0.61	-1.30	-0.59	11
T7	50%	-0.91	-0.57	-0.14	-0.63	12
T10	50%	-1.53	-1.19	-0.99	-1.30	13