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

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

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

• Cultivation·Physiology & Biochemistry • Previous Articles Next Articles

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 Online:2025-12-25 Published:2025-12-20
Contact: WANG Xiaofei, YU Kun

Abstract

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

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.

Figures/Tables 12

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

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

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

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

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

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

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

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

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

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

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

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

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