非结构性碳水化合物与氮分配对美洲黑杨和青杨耐盐能力的影响

doi:10.17521/cjpe.2021.0240

摘要/Abstract

摘要：

土壤盐渍化是阻碍林业发展的重要原因, 杨树(Populus spp.)是中国主要的人工林树种, 探究盐胁迫下植物的碳氮代谢特征与抗盐胁迫能力, 将有助于杨树人工林的可持续发展。该研究利用美洲黑杨(P. deltoides)和青杨(P. cathayana)两个物种, 采用去叶与不去叶处理, 在盐胁迫下研究两种杨树的抗逆性差异。研究发现, 盐胁迫下美洲黑杨的总生物量和光合能力均显著高于青杨。盐胁迫与去叶处理导致美洲黑杨叶绿素浓度和光系统II最大光量子效率显著高于青杨, 表明去叶对美洲黑杨影响较小, 但是加重了盐对青杨的毒害作用。美洲黑杨茎叶Na⁺浓度显著低于青杨, 表明美洲黑杨能够有效地限制Na⁺向地上部分运输。在盐胁迫条件下, 美洲黑杨茎和根比青杨能够维持更高浓度的淀粉、可溶性糖以及蔗糖, 前者较高的腺苷二磷酸葡萄糖焦磷酸化酶活性促进了光合产物向淀粉转换, 保证植物有充足的非结构性碳水化合物来参与渗透调节和维持其他生命活动, 而去叶使得青杨非结构性碳水化合物严重不足, 受盐胁迫影响更严重。盐胁迫下, 青杨分布在脂溶性蛋白(膜系统相关蛋白质)的氮浓度显著下降, 而NH₄⁺、谷氨酸脱氢酶活性与脯氨酸浓度显著升高。研究结果证明, 非结构性碳水化合物的积累、转化和分配是植物抗逆性的重要特征。

关键词: 非结构性碳水化合物, 渗透调节, 氮分配, 美洲黑杨, 青杨

Abstract:

Aims The increasing level of soil salinization has been one of the most important factors to limit the development of forestry. The fast-growing Populusspp. are widely used for tree plantations and afforestation around the world and play crucial role in economic and ecological functions. Linking carbon and nitrogen metabolism with the resistance to soil salinity stress, will help to well develop the Populus plantations in salinization area.

Methods The present study used P. deltoidesand P. cathayana for materials, while two salt (NaCl) concentrations and two defoliation treatments were applied. The carbon supply ability and allocation, nitrogen metabolism and allocation of the two poplar species were mainly investigated in different treatments.

Important findings We found that the P. deltoides had higher total biomass and photosynthetic rate than P. cathayana under salinity stress. The chlorophyll concentration and the PSII maximum photochemical efficiency of P. deltoides were significantly higher than those of P. cathayana especially under defoliation with salinity stress, which demonstrated stronger damage on P. cathayana. The defoliation treatment aggravated the damage of NaCl on P. cathayana. The Na⁺ concentration in leaf and stem of P. deltoides was significantly lower than that of P. cathayana under salinity stress, demonstrating that the P. deltoides strongly restricted Na⁺ up-transport from root. Stem and root of P. deltoides had higher concentrations of starch, soluble sugars and sucrose than P. cathayana under salinity stress. The higher adenosine diphosphate glucose pyrophosphorylase activity facilitated the production of starch in P. deltoides than in P. cathayana. The defoliation greatly reduced the resistant ability of P. cathayana to salinity because of lower supply of non-structural carbohydrate to osmoregulation function. The allocation of nitrogen to sodium dodecyl sulfate-soluble protein of P. cathayana was significantly reduced by increasing salt, whereas NH₄⁺ concentration, glutamate dehydrogenase activity and proline concentration were significantly higher than those of P. deltoides. Our results demonstrated the crucial role of non-structural carbohydrate of plant species in resisting soil salinity stress.

Key words: non-structural carbohydrate, osmoregulation, nitrogen allocation, Populus deltoides, Populus cathayana

林夏珍, 刘林, 董婷婷, 方琦博, 郭庆学. 非结构性碳水化合物与氮分配对美洲黑杨和青杨耐盐能力的影响. 植物生态学报, 2021, 45(9): 961-971. DOI: 10.17521/cjpe.2021.0240

LIN Xia-Zhen, LIU Lin, DONG Ting-Ting, FANG Qi-Bo, GUO Qing-Xue. Effects of non-structural carbohydrate and nitrogen allocation on the ability of Populus deltoides and P. cathayana to resist soil salinity stress. Chinese Journal of Plant Ecology, 2021, 45(9): 961-971. DOI: 10.17521/cjpe.2021.0240

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链接本文: https://www.plant-ecology.com/CN/10.17521/cjpe.2021.0240

https://www.plant-ecology.com/CN/Y2021/V45/I9/961

图/表 9

图1 不同处理下美洲黑杨和青杨茎生物量(A)、根生物量(B)、总生物量(C)和叶片特征(D)(平均值±标准误)。CK, 对照; D, 去叶; Sa, 盐胁迫; Sa-D, 盐胁迫与去叶; Sp, 物种。不同小写字母代表差异显著(p < 0.05)。**, 0.001 < p ≤0.01; ***, p ≤ 0.001。

Fig. 1 Stem biomass (A), root biomass (B), total biomass (C) and leaf performance (D) of Populus deltoides and P. cathayana under different treatments (mean ± SE). CK, control; D, defoliation; Sa, salt stress; Sa-D, salt stress and defoliation; Sp, species. Different lowercase letters indicate significant differences among treatments (p < 0.05). **, 0.001 < p ≤0.01; ***, p ≤ 0.001.

图2 不同处理下美洲黑杨和青杨叶、茎和根中Na+与Cl-浓度(平均值±标准误)。由于青杨盐胁迫与去叶组根系生物量不足, 所以未测定根系Cl-浓度。CK, 对照; D, 去叶; Sa, 盐胁迫; Sa-D, 盐胁迫与去叶; Sp, 物种。不同小写字母代表差异显著(p < 0.05)。*, 0.01 < p ≤ 0.05; **, 0.001 < p ≤ 0.01; ***, p ≤ 0.001。

Fig. 2 Na+ and Cl- concentrations of leaf, stem and root in both Populus deltoides and P. cathayana under different treatments (mean ± SE). Root Cl- concentration was not tested because the root biomass of P. cathayana in the salt stress and defoliation treatment was not sufficient. CK, control; D, defoliation; Sa, salt stress; Sa-D, salt stress and defoliation; Sp, species. Different lowercase letters indicate significant differences among treatments (p < 0.05). *, 0.01 < p ≤ 0.05; **, 0.001 < p ≤ 0.01; ***, p ≤ 0.001.

图3 不同处理下美洲黑杨和青杨叶片光合与荧光特征(平均值±标准误)。Fv/Fm, 最大光量子效率; gs, 气孔导度; Pn, 净光合速率; YII, 实际光量子效率。CK, 对照; D, 去叶; Sa, 盐胁迫; Sa-D, 盐胁迫与去叶; Sp, 物种。不同小写字母代表差异显著(p < 0.05)。*, 0.01 < p ≤ 0.05; **, 0.001 < p ≤ 0.01; ***, p ≤ 0.001。

Fig. 3 The leaf photosynthetic and chlorophyll fluorescence traits of Populus deltoides and P. cathayana under different treatments (mean ± SE). Fv/Fm, maximum yield of primary photochemistry; gs, stomatal conductance; Pn, net photosynthetic rate; YII, effective quantum yield of PSII. CK, control; D, defoliation; Sa, salt stress; Sa-D, salt stress and defoliation; Sp, species. Different lowercase letters indicate significant differences among treatments (p < 0.05). *, 0.01 < p ≤ 0.05; **, 0.001 < p ≤ 0.01; ***, p ≤ 0.001.

图4 不同处理下美洲黑杨和青杨叶、茎和根淀粉浓度(平均值±标准误)。CK, 对照; D, 去叶; Sa, 盐胁迫; Sa-D, 盐胁迫与去叶。不同小写字母代表差异显著(p < 0.05)。*, 0.01 < p ≤ 0.05; **, 0.001 < p ≤ 0.01; ***, p ≤ 0.001。

Fig. 4 Leaf, stem and root starch concentration of Populus deltoides and P. cathayana under different treatments (mean ± SE). CK, control; D, defoliation; Sa, salt stress; Sa-D, salt stress and defoliation; Sp, species. Different lowercase letters indicate significant differences among treatments (p < 0.05). *, 0.01 < p ≤ 0.05; **, 0.001 < p ≤ 0.01; ***, p ≤ 0.001.

表1 不同处理条件下美洲黑杨与青杨叶、茎和根中可溶性糖与蔗糖浓度(平均值±标准误)

Table 1 Soluble sugars and sucrose concentration of leaf, stem and root in both Populus deltoides and P. cathayana under different treatments (mean ± SE)

处理 Treatment	可溶性糖 Soluble sugars (mg·g^-1)			蔗糖 Sucrose (mg·g^-1)
处理 Treatment	叶 Leaf	茎 Stem	根 Root	叶 Leaf	茎 Stem	根 Root
美洲黑杨 P. deltoides
对照 Control (CK)	134.1 ± 4.4^a	71.2 ± 2.2^a	51.6 ± 1.3^b	75.6 ± 3.9^a	27.6 ± 1.9^ab	27.6 ± 1.4^b
去叶 Defoliation (D)	143.1 ± 4.6^a	58.4 ± 1.9^bc	33.0 ± 1.3^e	73.8 ± 4.3^a	26.5 ± 2.6^abc	19.3 ± 1.4^c
盐胁迫 Salt stress (Sa)	144.9 ± 6.0^a	67.2 ± 3.0^ab	60.3 ± 1.8^a	79.4 ± 5.8^a	35.0 ± 4.4^a	37.7 ± 3.2^a
盐胁迫与去叶 Salt stress and Defoliation (Sa-D)	149.0 ± 2.3^a	54.1 ± 1.6^c	45.1 ± 1.1^bc	75.4 ± 3.9^a	25.3 ± 3.2^abc	22.0 ± 1.4^bc
青杨 P. cathayana
CK	144.6 ± 3.4^a	59.7 ± 1.8^bc	39.4 ± 1.5^cd	61.0 ± 2.4^ab	27.0 ± 3.3^abc	19.4 ± 0.6^c
D	141.6 ± 1.1^a	44.4 ± 1.9^d	38.7 ± 2.0^cd	47.2 ± 2.8^b	17.8 ± 2.0^bc	21.2 ± 1.8^bc
Sa	113.6 ± 5.5^b	34.6 ± 1.4^e	29.9 ± 3.4^e	49.0 ± 8.1^b	15.2 ± 1.6^bc	14.5 ± 1.2^cd
Sa-D	113.0 ± 4.2^b	31.0 ± 1.1^e	18.5 ± 1.2^f	44.5 ± 3.4^b	14.6 ± 1.2^c	11.0 ± 1.4^d
p
物种 Species (Sp)	<0.001	<0.001	<0.001	<0.001	<0.001	<0.001
D	0.432	<0.001	<0.001	0.076	0.012	<0.001
Sa	0.001	<0.001	0.094	0.483	0.264	0.636
Sp × D	0.168	0.216	<0.001	0.352	0.894	<0.001
Sp × Sa	<0.001	<0.001	<0.001	0.138	0.010	<0.001
D × Sa	0.833	0.044	0.174	0.598	1.000	0.012
Sp × D × Sa	0.549	0.035	0.010	0.388	0.034	0.676

图5 不同处理下美洲黑杨和青杨叶、根中腺苷二磷酸葡萄糖(ADPG)焦磷酸化酶活性(平均值±标准误)。CK, 对照; D, 去叶; Sa, 盐胁迫; Sa-D, 盐胁迫与去叶; Sp, 物种。不同小写字母代表差异显著(p < 0.05)。*, 0.01 < p ≤ 0.05; **, 0.001 < p ≤ 0.01; ***, p ≤ 0.001。

Fig. 5 Adenosine diphosphate glucose (ADPG) pyrophosphorylase activity in the leaf and root of Populus deltoides and P. cathayana under different treatments (mean ± SE). CK, control; D, defoliation; Sa, salt stress; Sa-D, salt stress and defoliation; Sp, species. Different lowercase letters indicate significant differences among treatments (p < 0.05). *, 0.01 < p ≤ 0.05; **, 0.001 < p ≤ 0.01; ***, p ≤ 0.001.

图6 不同处理下美洲黑杨与青杨叶氮稳定同位素比值(δ15N)(平均值±标准误)。CK, 对照; D, 去叶; Sa, 盐胁迫; Sa-D, 盐胁迫与去叶; Sp, 物种。不同小写字母代表差异显著(p < 0.05)。*, 0.01 < p ≤ 0.05; **, 0.001 < p ≤ 0.01; ***, p ≤ 0.001。

Fig. 6 Nitrogen stable isotope ratio (δ15N) in leaves of Populus deltoides and P. cathayana under different treatments (mean ± SE). CK, control; D, defoliation; Sa, salt stress; Sa-D, salt stress and defoliation; Sp, species. Different lowercase letters indicate significant differences among treatments (p < 0.05). *, 0.01 < p ≤ 0.05; **, 0.001 < p ≤ 0.01; ***, p ≤ 0.001.

图7 不同处理下美洲黑杨和青杨叶与根中NH4+、NO3-和脯氨酸浓度(平均值±标准误)。CK, 对照; D, 去叶; Sa, 盐胁迫; Sa-D, 盐胁迫与去叶; Sp, 物种。不同小写字母代表差异显著(p < 0.05)。*, 0.01 < p ≤ 0.05; **, 0.001 < p ≤ 0.01; ***, p ≤ 0.001。

Fig. 7 NH4+, NO3- and proline concentrations in the leaf and root of Populus deltoides and P. cathayana under different treatments (mean ± SE). CK, control; D, defoliation; Sa, salt stress; Sa-D, salt stress and defoliation; Sp, species. Different lowercase letters indicate significant differences among treatments (p < 0.05). *, 0.01 < p ≤ 0.05; **, 0.001 < p ≤ 0.01; ***, p ≤ 0.001.

表2 不同处理条件下美洲黑杨与青杨叶和根谷氨酸脱氢酶与谷氨酰胺合成酶活性(平均值±标准误)

Table 2 Glutamate dehydrogenase (GDH) and glutamine synthase (GS) activity of leaf and root in both Populus deltoides and P. cathayana under different treatments (mean ± SE)

处理 Treatment	谷氨酸脱氢酶 GDH (U)		谷氨酰胺合成酶 GS (U)
	叶 Leaf	根 Root	叶 Leaf	根 Root
美洲黑杨 P. deltoides
对照 Control (CK)	202.1 ± 25.3^cd	63.7 ± 7.7^b	7.5 ± 1.7^a	5.3 ± 0.5
去叶 Defoliation (D)	111.6 ± 26.2^de	82.6 ± 4.9^b	9.5 ± 1.6^a	4.6 ± 0.4
盐胁迫 Salt stress (Sa)	411.9 ± 40.6^b	129.3 ± 9.3^a	11.3 ± 1.8^a	4.6 ± 0.4
盐胁迫与去叶 Salt stress and Defoliation (Sa-D)	685.1 ± 22.6^a	49.2 ± 9.4^b	13.7 ± 1.5^a	3.8 ± 0.2
青杨 P. cathayana
CK	114.6 ± 15.2^de	73.5 ± 7.1^b	7.2 ± 0.9^a	3.5 ± 0.3
D	58.3 ± 12.6^e	85.7 ± 9.1^b	7.9 ± 0.9^a	3.7 ± 0.9
Sa	248.8 ± 36.7^c	78.4 ± 11.4^b	4.1 ± 0.5^a	3.5 ± 0.2
Sa-D	248.1 ± 28.1^c	78.2 ± 11.2^b	5.8 ± 0.9^a	3.8 ± 0.2
p
物种 Spices (Sp)	<0.001	0.726	<0.001	0.004
D	0.114	0.063	0.078	0.491
Sa	<0.001	0.253	0.454	0.242
Sp × D	0.004	0.007	0.582	0.136
Sp × Sa	<0.001	0.181	0.001	0.216
D × Sa	<0.001	<0.001	0.736	0.920
Sp × D × Sa	<0.001	0.002	0.880	0.888

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