Morphological, photosynthetic physiological and transcriptome analyses of Pteroceltis tatarinowii in response to different nitrogen application levels

doi:10.12302/j.issn.1000-2006.202108019

JOURNAL OF NANJING FORESTRY UNIVERSITY ›› 2023, Vol. 47 ›› Issue (5): 87-96.doi: 10.12302/j.issn.1000-2006.202108019

Morphological, photosynthetic physiological and transcriptome analyses of Pteroceltis tatarinowii in response to different nitrogen application levels

GUO Wei¹(), HAN Xiu¹, ZHANG Li², WANG Ying¹, DU Hui¹, YAN Yu¹, SUN Zhongkui³, ZHANG Lin¹, LI Guohua¹^,^*(), LUO Lei¹^,^*()

1. Taishan Academy of Forestry Sciences, Tai’an 271000, China
2. College of Agricultural and Biological Engineering, Heze University, Heze 274015, China
3. Tai’an Time Garden Technology Development Co., Ltd, Tai’an, 271000, China

Received:2021-08-10 Revised:2022-07-12 Online:2023-09-30 Published:2023-10-10
Contact: LI Guohua,LUO Lei

Abstract

Abstract:

【Objective】Our objectives are to study the morphological and photosynthetic physiological changes of Pteroceltis tatarinowii under different nitrogen application levels, and screen nitrogen response related genes in order to provide reference for further research on the molecular mechanisms how nitrogen application trigger changes in P. tatarinowii. 【Method】A pot experiment was conducted with the cuttings of P. tatarinowii fertilized with Hocking’s complete nutrient solution with 0 (limiting, N₀), 2 (intermediate, N₂) and 50 mmol/L (luxuriant, N₅₀) NH₄NO₃, respectively. The physiological and photosynthetic morphological parameters were determined at day 28. SMRT-seq, performed with the pooled sample of P. tatarinowii treated with different nitrogen application levels, provided full length transcriptome data as a reference for the RNA-seq. Differentially expressed genes responding to different nitrogen levels were screened using bioinformatics methods. Then, the KEGG pathway enrichment analysis was conducted. The expression of the differentially expressed genes enriched in roots and leaves was quantified by RT-qPCR. 【Result】The physiological and morphological observations, determined at day 28 after being fertilized with different nitrogen application levels, showed that the values of height, stem diameter, number of leaves, leaf area, specific leaf area, biomass of leaves, biomass of stems, N concentration in roots, leaves and stems increased with the increase of nitrogen concentration, while the values of the total root length, total root surface area, total root volume, specific root length, root to shoot ratio, and biomass of roots, all decreased with the increase of nitrogen concentration. The chlorophyll a, chlorophyll b, carotenoid content, net photosynthetic rates and stomatal conductance were significantly promoted by the luxuriant nitrogen level. Of the differentially expressed genes among different nitrogen levels based on the global transcriptomic profiling by RNA-seq, 76 genes were up-regulated following the increase of nitrogen application levels, while 32 genes were opposite. The KEGG pathway enrichment analysis of the 108 genes showed that the top two pathways were photosynthesis and nitrogen metabolism. The photosynthesis pathway was enriched with OEE2, OEE3, PSBR, PSB27, PSAF and PSAK, while the nitrogen metabolism pathway was enriched with two NR genes and one NiR gene. The expression analysis showed that the nine genes were with similar expression patterns in roots and leaves, lowest expression levels in limiting nitrogen level while highest expression levels in luxuriant nitrogen. The expression levels of six genes of photosynthesis pathway in leaves were higher than that in roots under each nitrogen level. 【Conclusion】 Following the increase of nitrogen application levels, photosynthesis pathway genes were up-regulated, which promoted photosynthesis, while, nitrate reductase genes and nitrite reductase genes were up-regulated, which improved the nitrate assimilation efficiency. In the absence of a reference genome sequence, our results provided a basis for exploring the molecular mechanisms and discovering key candidate genes how nitrogen trigger changes in P. tatarinowii.

Key words: Pteroceltis tatarinowii, nitrogen, morphological and photosynthetic physiological response, full length transcriptome, differentially expressed gene

CLC Number:

S722.5

GUO Wei, HAN Xiu, ZHANG Li, WANG Ying, DU Hui, YAN Yu, SUN Zhongkui, ZHANG Lin, LI Guohua, LUO Lei. Morphological, photosynthetic physiological and transcriptome analyses of Pteroceltis tatarinowii in response to different nitrogen application levels[J]. JOURNAL OF NANJING FORESTRY UNIVERSITY, 2023, 47(5): 87-96.

Figures/Tables 8

Table 1

Table 2

Morphological and photosynthetic physiological features of P. tatarinowii to different nitrogen treatments"

指标 parameter	缺氮 N₀	中氮 N₂	高氮 N₅₀	显著性 significant
株高/cm height	85.35±1.43 c	91.68±2.27 b	101.52 ± 2.55 a	**
地径/mm stem diameter	4.79±0.11 c	4.99±0.09 b	5.22±0.07 a	**
叶片数量number of leaves	24.50±1.26 c	26.70±0.75 b	31.00±1.29 a	**
叶面积/cm² leaf area	46.95±2.4 c	50.21±1.53 b	59.30±2.17 a	**
比叶面积/(cm²·g^-1) specific leaf area	186.26±11.69 c	219.53±7.15 b	240.7 a±10.04 a	**
总根长/m total root length	60.12±4.90 a	49.88±4.20 b	39.85±2.88 c	**
总根表面积/cm² total root surface area	350.52±13.27 a	267.35±15.62 b	173.58±16.95 c	**
总根体积/cm³ total root volume	1.93±0.16 a	1.57±0.13 b	0.89±0.12 c	**
比根长/(m· g^-1) specific root length	23.98±0.59 a	22.63±0.39 b	16.57±0.76 c	**
根冠比root to shoot ratio	0.81±0.06 a	0.56±0.08 b	0.33±0.05 c	**
茎生物量/(g· 株^-1) biomass of stems	0.84±0.09 c	1.20±0.07 b	1.46±0.10 a	**
叶片生物量/(g· 株^-1) biomass of leaves	1.97±0.09 c	2.48±0.11 b	3.46±0.12 a	**
根系生物量/(g· 株^-1) biomass of roots	2.48±0.12 a	1.99±0.13 b	1.54±0.08 c	**
净光合速率/(μmol· m^-2·s^-1) net photosynthetic rates	11.26±0.75 c	14.13±0.66 b	17.91±0.90 a	**
气孔导度/(mol· m^-2·s^-1) stomatal conductance	0.46±0.04 c	0.54±0.06 b	0.62±0.05 a	*
蒸腾速率/(mmol· m^-2· s^-1) transpiration	5.79±0.12 b	6.56±0.10 a	6.56±0.14 a	**
叶绿素a含量/(mg· g^-1) chlorophyll a content	4.46±0.10 c	5.55±0.14 b	6.62±0.12 a	**
叶绿素b含量/(mg· g^-1) chlorophyll b content	1.74±0.08 c	2.30±0.12 b	2.62±0.06 a	**
类胡萝卜素含量/(mg·g^-1)carotenoid content	1.10±0.08 c	1.35±0.06 b	1.53±0.07 a	**
根系氮含量/(mg·g^-1) N content in roots	3.59±0.12 c	4.92±0.13 b	6.80±0.09 a	**
叶片氮含量/(mg·g^-1) N content in leaves	6.81±0.08 c	9.16±0.13 b	12.30±0.12 a	**
茎氮含量/(mg·g^-1) N content in stems	4.49±0.13 c	6.49±0.15 b	9.48±0.12 a	**

Table 2

Table 3

Table 4

Fig. 1

Fig. 2

Fig. 3

Table 5

Expression analysis of the nine differentially expressed genes in roots and leaves"

基因编号 gene ID	基因注释 gene description	RNA-seq表达量 (根) RNA-seq expression level in roots			荧光定量PCR表达量(根) RT-qPCR expression level in roots			荧光定量PCR表达量 (叶片) RT-qPCR expression level in leaves
基因编号 gene ID	基因注释 gene description	缺氮 (N₀)	中氮 (N₂)	高氮 (N₅₀)	缺氮 (N₀)	中氮 (N₂)	高氮 (N₅₀)	缺氮 (N₀)	中氮 (N₂)	高氮 (N₅₀)
Pt13441/f2p0/1188 Oxygen-evolving enhancer protein 2	氧增强蛋白基因2(OEE2)	6.35	13.05	23.17	1.00±0.06	4.62±0.21	15.12±0.50	3.47±0.48	5.09±0.30	20.60±4.74
Pt17935/f14p0/953	氧增强蛋白基因3 (OEE3) Oxygen-evolving enhancer protein 3	8.03	46.46	87.6	1.00±0.05	6.23±0.30	18.93±1.35	2.91±0.40	15.12±0.50	32.59±28.21
Pt21392/f10p0/756	光系统Ⅱ10kDa蛋白基因 (PSBR photosystem Ⅱ 10 kDa polypeptide, chloroplastic	47.83	151.77	305.11	1.00±0.06	5.46±0.14	18.73±2.39	2.14±0.12	18.93±1.35	41.23±1.59
Pt17952/f3p0/946	光系统Ⅱ修复蛋白(PSB27) photosystem Ⅱ repair protein PSB27-H1, chloroplastic	3.36	8.26	14.74	1.00±0.13	5.09±0.30	30.83±1.32	2.70±0.11	27.85±1.20	44.17±0.91
Pt18021/f3p0/940	光系统Ⅰ反应中心蛋白亚基Ⅲ(PSAF) photosystem I reaction center subunit Ⅲ, chloroplastic	1.93	5.51	16.88	1.00±0.07	3.37±0.09	22.22±0.65	2.88±0.07	30.83±1.32	88.05±4.18
Pt21940/f2p0/718	光系统Ⅰ反应中心蛋白亚基K (PSAK) photosystem I reaction center subunit psaK, chloroplastic-like	7.79	17.78	30.73	1.00±0.06	3.20±0.16	15.08±0.90	3.95±0.12	24.16±1.12	55.10±0.63
Pt10185/f2p0/1383	硝酸还原酶基因(NR) nitrate reductase	23.92	105.79	386.53	1.00±0.09	4.78±0.12	24.16±1.12	3.24±0.19	20.59±4.74	95.26±3.46
Pt527/f2p0/2771	硝酸还原酶基因(NR) nitrate reductase	32.58	192.52	827.61	1.00±0.06	8.42±0.75	26.98±0.94	4.59±0.21	11.91±0.82	25.04±1.46
Pt3975/f2p0/1900	亚硝酸还原酶基因(NiR) nitrite reductase	49.69	199.64	363.95	1.00±0.10	12.55±0.88	55.10±0.63	3.11±0.10	15.08±0.90	30.83±1.32

Table 5

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基因编号 gene ID	引物序列(正向/反向) primer sequences (forward/reverse)
Pt13441/f2p0/1188	GAAGGTGGGAAGCACCAACT/ ACCACCTCTTATCTCCGGCT
Pt17935/f14p0/953	TATGGCTTCAATGGCGGGTT/ TGACCATGTTCAAGCGGGTT
Pt21392/f10p0/756	ATGGTGGCATGGACTTGAGG/ CCCATCGACATTAGCACCGT
Pt17952/f3p0/946	GGGACTTCTTGTCCCTCGTG/ TTCTTCGTCCGAAGCTGCAT
Pt18021/f3p0/940	CAGATATCGCCGGACTGACC/ AGTCTTTTCGATCGTCGCGT
Pt21940/f2p0/718	CTCCCCCAATTCAATGGGCT/ GTAATCACACCGAGCACCCA
Pt10185/f2p0/1383	ATTGGCGAGCTTCTCACCTC/ CTGTCAAAATTGGCTGCGCT
Pt3975/f2p0/1900	TGGCAAATTCGTGGAGTGGT/ TTCCACTCTGCAGGCTTGTC
Pt527/f2p0/2771	ATTGGCGAGCTTCTCACCTC/ CTGTCAAAATTGGCTGCGCT
Pt12965/f6p0/1249	TGGGCTTTGAAGCAGCTTGT/ TCCTTGGTTGGTTCCCCTCT

名称term	数量amount
子读序数量 number of subread	23 007 808
子读序平均长度/bp average length of subread	1 098
子读序的N₅₀值/bp N₅₀ of subread	1 362
环形一致性序列数量 number of CCS	313 170
环形一致性序列的平均长度/bp average length of CCS	1 441
环形一致性序列的N₅₀值/bp N₅₀ of CCS	1 761
全长非嵌合序列数量 number of FLNC	219 220
全长非嵌合序列平均长度/bp average length of FLNC	1 171
校正一致性序列数量 number of PCS	29 644
校正一致性序列的平均长度/bp average length of PCS	1 197
校正一致性序列的N₅₀值/bp N₅₀ of PCS	1 461
基因数量 number of gene	11 801
基因序列的平均长度/bp average length of gene sequence	1 375
基因序列的N₅₀值/bp N₅₀ of gene sequence	1 628

生物学重复样本名称 biological replicates name	经过质控后的读序 clean reads	比对的读序 mapped reads	比对率/% mapping ratio
N₀_1	50 405 948	27 669 444	54.89
N₀_2	55 548 484	30 325 496	54.59
N₀_3	60 380 062	32 665 094	54.10
N₂_1	59 652 746	32 383 922	54.29
N₂_2	60 920 142	32 595 410	53.51
N₂_3	61 196 822	32 977 234	53.89
N₅₀_1	68 662 986	41 316 042	60.17
N₅₀_2	52 207 344	31 092 286	59.56
N₅₀_3	69 973 034	41 729 364	59.64
合计	538 947 568	302 754 292	56.18

Morphological, photosynthetic physiological and transcriptome analyses of Pteroceltis tatarinowii in response to different nitrogen application levels

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