低温对高山嵩草叶片光化学和非光化学能量耗散特征的影响

doi:10.17521/cjpe.2022.0227

植物生态学报 ›› 2023, Vol. 47 ›› Issue (10): 1441-1452.DOI: 10.17521/cjpe.2022.0227

低温对高山嵩草叶片光化学和非光化学能量耗散特征的影响

师生波¹^,⁴^,^*(), 师瑞², 周党卫¹^,³, 张雯⁴

¹中国科学院西北高原生物研究所, 中国科学院高原生物适应与进化重点实验室, 西宁 810001
²韶关生物经济高等研究院, 广东伯克生物医药有限公司, 广东韶关 512500
³青海民族大学药学院, 西宁 810007
⁴甘肃省治沙研究所, 甘肃省荒漠化与风沙灾害重点实验室培育基地, 兰州 730070

收稿日期:2022-06-06 接受日期:2022-10-10 出版日期:2023-10-20 发布日期:2023-11-23
通讯作者: * E-mail: sbshi@nwipb.cas.cn
基金资助:
青海省自然科学基金(2019-ZJ-7016);青海省创新平台建设专项(2017-ZJ-Y20);青海省创新平台建设专项(2021-ZJ-Y05)

Effects of low temperature on photochemical and non-photochemical energy dissipation of Kobresia pygmaea leaves

SHI Sheng-Bo¹^,⁴^,^*(), SHI Rui², ZHOU Dang-Wei¹^,³, ZHANG Wen⁴

¹Key Laboratory of Adaptation and Evolution of Plateau Biology, Northwest Institute of Plateau Biology, Chinese Academy of Sciences, Xining 810001, China
²Guangdong Berke Biomedical Co., Ltd., Shaoguan Institute of Biomedicine, Shaoguan, Guangdong 512500, China
³College of Pharmacy, Qinghai Nationalities University, Xining 810007, China
⁴Key Laboratory Breeding Base of Desertification and Aeolian Sand Disaster Combating, Gansu Desert Control Research Institute, Lanzhou 730070, China

Received:2022-06-06 Accepted:2022-10-10 Online:2023-10-20 Published:2023-11-23
Supported by:
Natural Science Foundation of Qinghai Province(2019-ZJ-7016);Construction Project for Innovation Platform of Qinghai Province(2017-ZJ-Y20);Construction Project for Innovation Platform of Qinghai Province(2021-ZJ-Y05)

摘要/Abstract

摘要：

低温是青藏高原地区植物生长季内频繁发生的非生物胁迫, 然而其对典型高山植物叶片光能利用和分配的影响如何, 尚缺乏研究。该研究以高寒草甸优势种高山嵩草(Kobresia pygmaea)为材料, 采用叶绿素荧光成像分析技术, 研究了低温对光系统II (PSII)光化学及非光化学猝灭中光诱导和非光诱导的量子产量相对份额的影响。结果表明: PSII最大光化学量子效率(F_v/F_m和1/F_o - 1/F_m)的最适温度在10 ℃左右, 且变异系数(CV)较小; PSII相对电子传递速率(rETR)的光响应曲线随温度降低而整体下移, 其初始斜率(α)也相应降低。低温逆境可引起PSII实际光化学量子效率(Φ_PSII)和非光化学猝灭中非调节性能量耗散量子产量(Φ_NO)的降低, 及调节性能量耗散量子产量(Φ_NPQ)的增大, 并导致均值CV的增高。1 000 µmol·m⁻²·s⁻¹稳态光强下, Φ_PSII、Φ_NPQ和Φ_NO三组分的相对比率在20、10、5、0和-5 ℃分别为: 23:57:20、18:63:19、15:68:17、11:75:14和8:80:12。PSII反应中心光化学效率的相对限制(L_PPFD)随温度降低而逐渐增大, 且光强越大其限制增强。一般线性模型的双因素方差分析表明, PSII光化学和非光化学能量耗散过程没有交互效应产生。尽管光化学能量转换和保护性的调节机制可有效分配激发能, 能避免Φ_NO的增加, 但高山嵩草叶片的光合机构在维持运行的同时依然承受着来自低温的胁迫, 是影响植物光合生理过程及限制生长发育的重要因素。

关键词: 低温逆境, 光系统II非光化学猝灭, 高山嵩草, 青藏高原, 叶绿素荧光

Abstract:

Aims Kobresia pygmaea is a typical low temperature-tolerant arid mesophyte, and mainly distributes at low slope and high mountains ranging from 3 000 to 5 960 m on the Qingzang Plateau. Low temperature is a frequently occurring abiotic stress factor during the plants growing season on the Qingzang Plateau. The objectives of this study were to analyze the photochemical and non-photochemical energy distribution characteristics of the photosystem II (PSII) reaction center of K. pygmaea leaves, and explore their quenching protection mechanism in response to low temperature stress.

Methods Turf blocks (30 cm × 30 cm) of K. pygmaea meadow were collected from the Alpine Grassland Ecosystem Research Station of the Resource of Three Rivers, moved and kept in a culture room with air temperature of 24 °C/18 °C (day/night) at a diurnal photoperiod of 12 h and relative humidity of 45%; being irradiated with artificial LED light source of 500 µmol·m⁻²·s⁻¹ light intensity. When the turf black had been kept in culture room for one day, the measurements of chlorophyll fluorescence were performed immediately using chlorophyll fluorescence imager with built-in protocol. The trial of light response curves at different leaf temperatures, temperature response at a steady-state light intensity and light-temperature interaction effects were performed at controlled temperature using thermostatic control instruments. Based on the “Lake Model”, the relative variation of the PSII actual photochemical efficiency (Φ_PSII), the quantum yield of regulated energy dissipation (Φ_NPQ) and non-regulated energy dissipation (Φ_NO) were investigated. Furthermore, the interaction effects of low temperature and high light intensity was analyzed by two-way ANOVA of the general linear model (GLM).

Important findings The maximum quantum efficiency of PSII photochemistry (F_v/F_m and 1/F_o - 1/F_m) were higher at 10 °C and their coefficient of variation (CV) was smaller relative to other temperatures. The rapid light-response curves of the PSII relative electron transfer rate (rETR) showed a downward as a whole with the decreasing of temperature, and their initial slope (α) also decreased accordingly. Low temperature caused a decrease in Φ_PSII and Φ_NO, and an increase in Φ_NPQ, accompanied with enhancement of CV values. Under 1 000 µmol·m⁻²·s⁻¹ steady-state light intensity, the relative ratios of Φ_PSII:Φ_NPQ:Φ_NO at the temperature of 20, 10, 5, 0, and -5 °C were in turn 23:57:20, 18:63:19, 15:68:17, 11:75:14, and 8:80:12, showing remarkable decrease in Φ_PSII and increase in Φ_NPQ. The relative limitation of PSII photochemical efficiency (L_PPFD) increased gradually with the increase of light intensity, and also with the decrease of temperature. The two-way ANOVA of GLM showed that there were no interaction effects of low temperature and high light intensity in both PSII photochemical and non-photochemical energy dissipation processes. Therefore, the excited energy absorbed by PSII antenna pigments can be transferred and dissipated effectively by the photochemical energy conversion of Φ_PSII and protective regulatory mechanisms of Φ_NPQ avoiding the exacerbation of Φ_NO, which exhibited a strong tolerance and adaptation to alpine habitats. However, the increased instability of photosynthetic activities at low temperatures indicated that the photosynthetic apparatus of K. pygmaea still suffer the stress while maintaining normal operation. It can be inferred that the low temperature is an important factor affecting the photosynthetic physiological process and limiting growth and development and its distribution.

Key words: low-temperature stress, photosystem II non-photochemical quenching, Kobresia pygmaea, Qingzang Plateau, chlorophyll fluorescence

师生波, 师瑞, 周党卫, 张雯. 低温对高山嵩草叶片光化学和非光化学能量耗散特征的影响. 植物生态学报, 2023, 47(10): 1441-1452. DOI: 10.17521/cjpe.2022.0227

SHI Sheng-Bo, SHI Rui, ZHOU Dang-Wei, ZHANG Wen. Effects of low temperature on photochemical and non-photochemical energy dissipation of Kobresia pygmaea leaves. Chinese Journal of Plant Ecology, 2023, 47(10): 1441-1452. DOI: 10.17521/cjpe.2022.0227

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链接本文: https://www.plant-ecology.com/CN/10.17521/cjpe.2022.0227

https://www.plant-ecology.com/CN/Y2023/V47/I10/1441

图/表 9

图1 高山嵩草草甸及植株构型。A, 高山嵩草-杂类草草甸。B, 高山嵩草的垫状聚集生长方式。C, 发达的根系主要分布在10 cm深的土层, 与土壤形成致密的草根盘结层。D, 短粗根状茎及具密集褐色宿存叶鞘的植株。

Fig. 1 Kobresia pygmaea meadow and plant configuration. A, Natural landscape of K. pygmaea-forb meadow. B, Cushion aggregation growth pattern of K. pygmaea. C, Developed root system is mainly distributed within a depth of 10 cm, forming a dense layer with the soil. D, Plants with stubby rhizomes and dense brown persistent leaf sheaths.

图2 温度对高山嵩草叶片光系统II相对电子传递速率(rETR)快速光响应曲线的影响(平均值±标准差, n = 60)。

Fig. 2 Effects of measurement temperature on rapid light- response curves of the relative electron transfer rate through photosystem II (rETR) of Kobresia pygmaea leaves (mean ± SD, n = 60). PPFD, photosynthetical active photon flux density.

图3 高山嵩草叶片光系统II最大光化学量子效率(Fv/Fm和1/Fo - 1/Fm)的温度响应。图中不同小写字母表示Fv/Fm和1/Fo - 1/Fm在不同测定温度间的差异显著(α = 0.05; 平均值±标准差, n = 60)。

Fig. 3 Response of the maximum quantum efficiency of photosystem II photochemistry (Fv/Fm and 1/Fo - 1/Fm) of Kobresia pygmaea leaves to temperature. Different lowercase letters indicate significant differences of Fv/Fm and 1/Fo - 1/Fm among different measurement temperature degree, respectively (α = 0.05; mean ± SD, n = 60).

图4 高山嵩草叶片光系统II非光化学猝灭系数(qNP)的温度响应及在不同稳态作用光强的变化。A中不同小写字母表示降温测定中1 000 μmol·m-2·s-1稳态光强下各温度间差异显著(α = 0.05; 平均值±标准差, n = 55); B中不同小写字母表示相同稳态光强时各温度间差异显著(α = 0.05; 平均值±标准差, n = 80)。

Fig. 4 Response of the photosystem II non-photochemical quenching coefficient (qNP) in Kobresia pygmaea leaves to temperature and its variation to steady-state light intensities. Different lowercase letters in A indicate significant differences among different measurement temperature under 1 000 μmol·m-2·s-1 steady-state light intensity (α = 0.05; mean ± SD, n = 55); different lowercase letters in B indicate significant differences among different temperature under the same steady-state light intensity (α = 0.05; mean ± SD, n = 80). PPFD, photosynthetical active photon flux density.

图5 温度对光系统II实际光化学量子效率(ΦPSII) (A)、调节性能量耗散量子产量(ΦNPQ) (B)和非调节性能量耗散量子产量(ΦNO) (C)相对份额的影响。不同小写字母表示ΦPSII、ΦNPQ和ΦNO在1 000 μmol·m-2·s-1稳态光强下不同温度间的差异显著(α = 0.05; 平均值±标准差, n = 55)。

Fig. 5 Effects of temperature on the photosystem II actual photochemical efficiency (ΦPSII) (A), the quantum yield of regulated energy dissipation (ΦNPQ) (B) and non-regulated energy dissipation (ΦNO) (C) in Kobresia pygmaea leaves. Different lowercase letters indicate significant differences among different measurement temperature under 1 000 μmol·m-2·s-1 steady-state light intensity (α = 0.05; mean ± SD, n = 55).

图6 不同测定温度下光系统II实际光化学量子效率(ΦPSII) (A)、调节性能量耗散量子产量(ΦNPQ) (B)和非调节性能量耗散量子产量(ΦNO) (C)相对份额的变化及对稳态作用光强的响应。不同小写字母表示同一稳态光强下ΦPSII、ΦNPQ和ΦNO在不同测定温度间的差异显著(α = 0.05; 平均值±标准差, n = 80)。

Fig. 6 Photosystem II actual photochemical efficiency (ΦPSII) (A), the quantum yield of regulated energy dissipation (ΦNPQ) (B), and non-regulated energy dissipation (ΦNO) (C) in Kobresia pygmaea leaves under different temperature degrees. Different lowercase letters indicate significant differences among measurement temperature degrees at the same light intensity (α = 0.05; mean ± SD, n = 80). PPFD, photosynthetical active photon flux density.

图7 高山嵩草叶片光系统II反应中心光化学效率的相对限制(LPPFD)的温度响应及在不同稳态作用光强的变化。A中不同小写字母表示1 000 μmol·m-2·s-1稳态光强下不同温度间差异显著(α = 0.05; 平均值±标准差, n = 55); B中不同小写字母表示相同稳态光强时不同温度间差异显著(平均值±标准差, n = 80)。

Fig. 7 Response of the relative limitation of photosystem II photochemical efficiency (LPPFD) in Kobresia pygmaea leaves to measurement temperature and their variation with steady-state light intensities. Different lowercase letters in A indicate significant differences among different temperature under 1 000 μmol·m-2·s-1 steady-state light intensity (mean ± SD, n = 55); different lowercase letters in B indicate significant differences among different measurement temperature under the same steady-state light intensity (α = 0.05; mean ± SD, n = 80). PPFD, photosynthetical active photon flux density.

图8 高山嵩草叶片光系统II反应中心开放比率(qL)的温度响应及在不同稳态作用光强的变化。A中不同小写字母表示1 000 μmol·m-2·s-1稳态光强下不同温度间差异显著(α = 0.05; 平均值±标准差, n = 55); B中不同小写字母表示相同稳态光强时不同温度间差异显著(α = 0.05; 平均值±标准差, n = 80)。

Fig. 8 Response of the fraction of open photosystem II centers (qL) in Kobresia pygmaea leaves to measurement temperature and their variation to steady-state light intensities. Different lowercase letters in A indicate significant differences among different measurement temperature under 1 000 μmol·m-2·s-1 steady-state light intensity (α = 0.05; mean ± SD, n = 55); different lowercase letters in B indicate significant differences among different measurement temperature under the same steady-state light intensity (α = 0.05; mean ± SD, n = 80). PPFD, photosynthetical active photon flux density.

表1 强光和低温胁迫处理间高山蒿草叶绿素荧光参数的交互效应分析

Table 1 Interaction effects analysis of high light intensity and low temperature on chlorophyll fluorescence parameters of kobresia pygmaea

	PPFD			低温 Low temperature			PPFD ×低温 PPFD × Low temperature
	F	p	η²	F	p	η²	F	p	η²
q_L	264.712	0	0.358	7.927	0	0.032	0.927	0.397	0.004
q_NP	163.739	0	0.257	23.102	0	0.089	0.848	0.429	0.004
Φ_PSII	417.730	0	0.468	22.572	0	0.087	0.948	0.388	0.004
Φ_NO	0	0.991	0	5.569	0.004	0.023	0.707	0.493	0.003
Φ_NPQ	476.751	0	0.501	33.935	0	0.125	0.788	0.455	0.003
rETR	174.423	0	0.269	24.480	0	0.094	0.276	0.759	0.001
L_PPFD	417.730	0	0.468	22.572	0	0.087	0.948	0.388	0.004

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低温对高山嵩草叶片光化学和非光化学能量耗散特征的影响

Effects of low temperature on photochemical and non-photochemical energy dissipation of Kobresia pygmaea leaves

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