施氮对苹果接穗叶片光合和内生菌特性的影响

doi:10.16420/j.issn.0513-353x.2024-0998

园艺学报 ›› 2025, Vol. 52 ›› Issue (12): 3303-3321.doi: 10.16420/j.issn.0513-353x.2024-0998

施氮对苹果接穗叶片光合和内生菌特性的影响

张换换¹, 李旭娇¹, 姚东东¹, 张光鑫¹, 葸金山¹, 梁银池¹, 赵丰云¹, 郁松林¹, 王小非²^,^*(), 于坤¹^,^*()

¹ 石河子大学农学院，新疆生产建设兵团特色果蔬栽培生理与种质资源利用兵团重点实验室，新疆石河子832000
² 山东农业大学园艺科学与工程学院，作物生物学国家重点试验室，山东果蔬优质高效生产协同创新中心，山东泰安271018

收稿日期:2025-04-02 修回日期:2025-10-13 出版日期:2025-12-25 发布日期:2025-12-20
通讯作者:
*（E-mail：yukun410@163.com，
xfwang1004@163.com）
基金资助:
新疆苹果产业技术体系建设专项项目(XJLGCYJSTX04-2024); 新疆生产建设兵团重点科技攻关项目(2024AB038)

Effects of Nitrogen Application on Leaf Photosynthetic and Endophyte Characteristics of Apple Scions

ZHANG Huanhuan¹, LI Xujiao¹, YAO Dongdong¹, ZHANG Guangxin¹, XI Jinshan¹, LIANG Yinchi¹, ZHAO Fengyun¹, YU Songlin¹, WANG Xiaofei²^,^*(), YU Kun¹^,^*()

¹ Key Laboratory of Special Fruits and Vegetables Cultivation Physiology and Germplasm Resources Utilization of Xinjiang Production and Construction Corps，Agricultural College，Shihezi University，Shihezi，Xinjiang 832000，China
² Shandong Collaborative Innovation Center for Fruit and Vegetable Production with High Quality and Efficiency，State Key Laboratory of Crop Biology，College of Horticulture Science and Engineering，Shandong Agricultural University，Tai’an，Shandong 271018，China

Received:2025-04-02 Revised:2025-10-13 Published:2025-12-25 Online:2025-12-20

摘要/Abstract

摘要：

以新疆野苹果[Malus sieversii（Ledeb.）Roem.]为砧木，分别嫁接新疆野苹果、‘寒富’（Malus × domestica Borkh.‘Hanfu’）和‘富士’（M. × domestica Borkh.‘Fuji’），设不施氮与施氮（0.2 g · kg^-1土）处理，采用稳定同位素示踪和高通量测序技术，测定接穗的叶片组织结构、光合特性、碳氮含量和内生菌群落结构的变化特征，探究氮素调控对苹果接穗叶片生理及内生微生物协同适应性的影响机制。结果表明，不施氮条件下‘富士’的叶片厚度、叶绿素含量和碳氮比均显著高于‘寒富’和新疆野苹果；施氮后‘寒富’的叶片净光合速率和气孔导度分别显著提高24.84%和73.86%，且其光合效率显著优于其他两种接穗。叶片内生菌群落分析表明，‘寒富’表现出最高的细菌和真菌群落多样性和丰富度，施氮处理进一步提升了其内生细菌群落的多样性指数（Chao1和Shannon指数分别增加7.30%和61.96%）和网络复杂性（节点数为598，链接数为75 728）。此外，施氮处理显著促进了‘寒富’叶片中功能有益菌属的富集，其中芽孢杆菌属（Bacillus）、新鞘氨醇单胞菌属（Novosphingobium）和鞘氨醇单胞菌属（Sphingomonas）的相对丰度分别较不施氮处理显著提高了226.21%、59.35%和149.42%。综上，氮素施用可显著改善苹果接穗叶片的光合特性并优化内生菌群落结构，其中‘寒富’接穗在氮素充足条件下表现出更优的光合性能和更稳定的内生菌群落。

关键词: 苹果, 新疆野苹果, 接穗, 施氮, 光合特性, 稳定同位素, 内生菌

Abstract:

To explore the mechanisms underlying nitrogen-mediated regulation of scion leaf adaptation，three apple scion varieties—Malus sieversii（Ledeb.）Roem.，‘Hanfu’（M. × domestica Borkh.）， and‘Fuji’（M. × domestica Borkh）were grafted onto M. sieversii rootstocks and subjected them to nitrogen-deficient and nitrogen-supplemented（0.2 g · kg^-1）conditions. Stable isotope tracing and high-throughput sequencing were employed to analyze variations in leaf tissue structure，photosynthetic characteristics，carbon and nitrogen content，and endophytic microbial communities among the different scion varieties. Under nitrogen-deficient conditions，‘Fuji’scion leaves exhibited significantly greater leaf thickness，chlorophyll content，and carbon-to-nitrogen ratio compared to‘Hanfu’and M. sieversii. Following nitrogen application，‘Hanfu’scion leaves showed a substantial increase in net photosynthetic rate and stomatal conductance by 24.84% and 73.86%，respectively，exhibiting superior photosynthetic efficiency over the other scions. Analysis of endophytic microbial communities revealed that‘Hanfu’scion leaves possessed the highest diversity and richness of bacterial and fungal communities，with nitrogen supplementation further enhancing the diversity indices（Chao1 and Shannon indices increased by 7.30% and 61.96%，respectively）and microbial network complexity（598 nodes and 75 728 edges）. Additionally，nitrogen application significantly promoted the enrichment of beneficial functional bacteria in‘Hanfu’scion leaves，with Bacillus，Novosphingobium，and Sphingomonas increasing in relative abundance by 226.21%，59.35%，and 149.42%，respectively，compared to the nitrogen-deficient condition. In conclusion，nitrogen application significantly improved the photosynthetic performance and optimized the endophytic microbial community structure of apple scion leaves. Among the tested scions，‘Hanfu’exhibited the most pronounced advantages under nitrogen-sufficient conditions，characterized by superior photosynthetic efficiency and a more stable endophytic microbiome. The findings highlight that nitrogen not only enhances the photosynthetic traits of apple scions but also regulates endophytic microbial composition，thereby enhancing environmental adaptability and growth potential.

Key words: apple, Malus sieversii, scions, nitrogen application, photosynthetic characteristics, stable isotopes, endophyte

张换换, 李旭娇, 姚东东, 张光鑫, 葸金山, 梁银池, 赵丰云, 郁松林, 王小非, 于坤. 施氮对苹果接穗叶片光合和内生菌特性的影响[J]. 园艺学报, 2025, 52(12): 3303-3321.

ZHANG Huanhuan, LI Xujiao, YAO Dongdong, ZHANG Guangxin, XI Jinshan, LIANG Yinchi, ZHAO Fengyun, YU Songlin, WANG Xiaofei, YU Kun. Effects of Nitrogen Application on Leaf Photosynthetic and Endophyte Characteristics of Apple Scions[J]. Acta Horticulturae Sinica, 2025, 52(12): 3303-3321.

图/表 12

图1 新疆野苹果嫁接不同接穗幼树13C和15N同位素标记示意图 CK：不施氮；AN：施氮。下同

Fig. 1 Schematic diagram of 13C and 15N isotope labeling of young trees grafted with different scions on Malus sieversii CK：No nitrogen applied，AN：Nitrogen applied. The same below

图2 施氮对新疆野苹果不同接穗叶片解剖结构的影响 UEC：上表皮细胞；LEC：下表皮细胞；PP：栅栏组织，SP：海绵组织

Fig. 2 Effect of nitrogen application on leaf anatomy of different apple scions of Malus sieversii UEC：Upper epidermal cells；LEC：Lower epidermal cells；PP：Palisade parenchyma；SP：Spongy parenchyma

表 1 施氮对不同苹果接穗叶片解剖结构特征的影响

Table 1 Effect of nitrogen application on leaf anatomical and structural characteristics of different apple scions

处理 Treatment	叶片厚度/μm Leaf thickness	上表皮厚度/μm Upper epidermal thickness	下表皮厚度/μm Lower epidermal thickness	栅栏组织厚度/μm Palisade parenchyma thickness	海绵组织厚度/μm Spongy parenchyma thickness
MS-CK	136.50 ± 3.03 e	11.07 ± 0.26 b	9.43 ± 0.12 a	45.57 ± 0.92 d	63.20 ± 3.12 c
MS-AN	169.43 ± 2.85 b	9.87 ± 0.25 c	9.10 ± 0.14 ab	73.80 ± 3.91 bc	74.17 ± 5.36 ab
HF-CK	152.37 ± 3.08 d	8.83 ± 0.19 d	8.60 ± 0.14 b	68.33 ± 0.85 c	61.53 ± 1.07 c
HF-AN	180.80 ± 3.89 a	11.90 ± 0.22 a	9.00 ± 0.24 ab	82.50 ± 5.17 a	73.70 ± 2.14 ab
FJ-CK	162.00 ± 4.11 c	11.63 ± 0.37 a	8.87 ± 0.45 ab	77.60 ± 2.68 ab	66.73 ± 4.14 bc
FJ-AN	175.39 ± 1.29 ab	11.67 ± 0.17 a	7.97 ± 0.31 c	76.03 ± 4.29 abc	77.30 ± 2.08 a
F值 F-value
接穗Scion (S)	29.518^***	32.371^***	10.522^**	31.399^***	1.927
氮素Nitrogen (N)	187.173^***	19.112^***	3.360	48.204^***	34.611^***
S × N	9.763^**	76.571^***	6.167^*	19.275^***	0.063

图3 施氮对不同苹果接穗叶片色素含量的影响 MS：新疆野苹果；HF：寒富；FJ：富士；CK：不施氮；AN：施氮。不同小写字母表示处理间差异显著（P < 0.05），下同

Fig. 3 Effect of nitrogen application on leaf pigment content of different apple scions MS：Malus sievesii；HF：Hanfu；FJ：Fuji；CK：No nitrogen applied；AN：Nitrogen applied. Different lowercase letters on the same day in the figure indicate significant differences between treatments（P < 0.05）. The same below

图4 施氮对不同苹果接穗叶片光合参数的影响

Fig. 4 Effect of nitrogen application on leaf photosynthetic parameters of different apple scions

图5 施氮对不同苹果接穗叶片碳和氮含量的影响 S：接穗，N：氮素。*、**和***分别表示在P < 0.05、0.01和0.001水平差异显著；ns表示无显著差异。下同

Fig. 5 Effect of nitrogen application on leaf carbon and nitrogen content of different apple scions S：Scion，N：Nitrogen. *，** and *** indicate significant differences at P < 0.05，0.01 and 0.001 levels，respectively；ns indicates no significant difference. The same below

图6 施氮对不同苹果接穗叶片内生菌群落多样性的影响

Fig. 6 Effect of nitrogen application on the diversity of leaf endophyte communities of different apple scions

图7 施氮对不同苹果接穗叶片内生优势菌门和属的影响

Fig. 7 Effect of nitrogen application on leaf endophytic dominant phyla and genera in different apple scions

图8 施氮对不同苹果接穗叶片内生细菌和真菌共现网络的影响

Fig. 8 Effect of nitrogen application on leaf endophytic bacterial and fungal co-occurrence networks in different apple scions

表 2 施氮对不同苹果接穗叶片内生细菌和真菌群落网络拓扑结构的影响

Table 2 Effect of nitrogen application on the network topology of leaf endophytic bacterial and fungal communities of different apple scions

微生物组 Microbiome	处理 Treatment	节点数 Total nodes	链接数 Total links	平均度 Average degree	密度 Density	正相关/% Positive	负相关/% Negative
细菌 Bacteria	MS-CK	182	4 270	46.92	0.259	98.67	1.33
	MS-AN	427	24 398	114.28	0.268	98.88	1.12
	HF-CK	367	16 922	92.22	0.252	98.78	1.22
	HF-AN	598	75 728	253.27	0.424	99.75	0.25
	FJ-CK	236	6 831	57.89	0.246	94.38	5.62
	FJ-AN	114	1 532	26.88	0.238	97.58	2.42
真菌 Fungi	MS-CK	78	695	17.82	0.231	90.94	9.06
	MS-AN	88	703	15.98	0.184	87.48	12.52
	HF-CK	109	1 437	26.37	0.244	97.70	2.30
	HF-AN	73	955	26.16	0.363	95.81	4.19
	FJ-CK	82	822	20.05	0.248	97.20	2.80
	FJ-AN	47	194	8.26	0.179	80.41	19.59

图9 叶片生理特性与内生细菌和真菌群落多样性和组成之间相关性 LT：叶片厚度，PPT：栅栏组织厚度，SPT：海绵组织厚度，Car：类胡萝卜素含量，Chl：叶绿素含量，Pn：净光合速率，Gs：气孔导度，CC：碳含量，NC：氮含量，C/N：碳氮比，13CC：13C含量，15NC：15N含量，13C/15N：13C/15N。叶片生理特性间用皮尔逊（Pearson）相关性分析；*、**和**分别表示在0.05、0.01和0.001水平显著相关。叶片生理因子与内生细菌和真菌群落多样性和组成用曼特尔（Mantel）相关分析

Fig. 9 Correlation analysis between leaf physiological properties and the diversity and composition of endophytic bacterial and fungal communities LT is leaf thickness，PPT is the palisade parenchyma thickness，SPT is the spongy parenchyma thickness thickness，Car is the carotenoid content，Chl is the chlorophyll content，Pn is the net photosynthetic rate，Gs is the stomatal conductance，CC is the carbon content，NC is the nitrogen content，C/N is the carbon to nitrogen ratio，13CC is the 13C content，15NC is the 15N content，and 13C/15N is the 13C to 15N ratio. Pearson correlation analysis was performed among leaf physiological traits；*，** and *** indicates significant correlation at the 0.05，0.01 and 0.001 levels，respectively. Mantel correlation analysis was used to evaluate the relationships between leaf physiological factors and the diversity and composition of endophytic bacterial and fungal communities

图10 叶片生理特性与内生细菌和真菌群落特征之间斯皮尔曼相关性分析 LT：叶片厚度，PPT：栅栏组织厚度，SPT：海绵组织厚度，Car：类胡萝卜素含量，Chl：叶绿素含量，Pn：净光合速率，Gs：气孔导度，CC：碳含量，NC：氮含量，C/N：碳氮比，13CC：13C含量，15NC：15N含量，13C/15N：13C/15N。*和**分别表示在0.05和0.01水平显著相关

Fig. 10 Sperman correlation analysis between leaf physiological properties and endophytic bacterial and fungal communities characteristics LT is leaf thickness，PPT is the palisade parenchyma thickness，SPT is the spongy parenchyma thickness thickness，Car is the carotenoid content，Chl is the chlorophyll content，Pn is the net photosynthetic rate，Gs is the stomatal conductance，CC is the carbon content，NC is the nitrogen content，C/N is the carbon to nitrogen ratio，13CC is the 13C content，15NC is the 15N content，and 13C/15N is the 13C to 15N ratio. * and ** indicates significant correlation at the 0.05 and 0.01 levels，respectively

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施氮对苹果接穗叶片光合和内生菌特性的影响

Effects of Nitrogen Application on Leaf Photosynthetic and Endophyte Characteristics of Apple Scions

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施氮对苹果接穗叶片光合和内生菌特性的影响

Effects of Nitrogen Application on Leaf Photosynthetic and Endophyte Characteristics of Apple Scions

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