亚热带地区3种常绿阔叶植物冬季光保护机制的差异

doi:10.17521/cjpe.2024.0258

摘要/Abstract

摘要：

越冬期常绿植物因光能吸收与利用的不平衡而造成冬季光抑制伤害, 虽然对于温带和北方冰冻环境下常绿植物冬季光保护策略已有许多研究, 但对不同耐冷性的常绿阔叶植物叶片光保护机制对亚热带零上低温为主的冬季低温的响应却了解有限。该研究选取栽培于亚热带的红叶石楠(Photinia × fraseri, 耐冷性强)、荷花木兰(Magnolia grandiflora, 耐冷性中等)和雅榕(Ficus concinna, 冷敏感)为材料, 对这3种常绿阔叶植物阴生叶和阳生叶光系统II (PSII)和光系统I (PSI)功能从秋季至翌年春季的变化展开研究。结果表明: 3种常绿阔叶植物阴生叶和阳生叶PSII和PSI光抑制及其光保护途径对冬季低温和初春升温表现出不同的温度响应特征。冬季低温强光仅造成红叶石楠阳生叶PSII轻微可逆光抑制, 但导致荷花木兰和雅榕阳生叶PSII和PSI严重光抑制, 并且雅榕PSII最大光化学效率(F_v/F_m)和PSI反应中心P700最大荧光信号(P_m)的下降幅度明显大于荷花木兰。红叶石楠阳生叶在冬季可通过增强热耗散(NPQ)和围绕PSI的环式电子传递(CEF-PSI)保护PSII和PSI, 且冬季低温强光刺激了阳生叶PSII和PSI功能产生补偿现象, 其PSII反应中心开放程度(q_P)、PSII和PSI光化学量子产量((Y(II)和(Y(I))在进入初春升温期(2023年3月)后可迅速恢复至高于秋季(2022年10月)的水平。荷花木兰阳生叶PSII和PSI功能在冬季持续下降, 但采用了增强CEF-PSI和保持相对较强的热耗散能力的光保护策略以维持PSII和PSI功能的协同性。而冬季的雅榕阳生叶虽然CEF-PSI得到增强, 但热耗散能力大幅下降, 低温强光对PSII和PSI造成严重伤害。亚热带冬季低温并未对3种植物阴生叶造成明显光抑制伤害。冬季的红叶石楠和荷花木兰阴生叶仅PSI发生轻微可逆光抑制, 其中红叶石楠主要通过部分关闭PSII反应中心以减少光能吸收和维持相对较高的光化学能力的光保护机制, 而荷花木兰则主要采用增强CEF-PSI与热耗散能力的光保护机制。冬季低温虽然降低了雅榕阴生叶热耗散能力, 但其PSII和PSI功能并未受到明显影响, 冬季低温仅导致雅榕阴生叶PSII和PSI轻微可逆光抑制。该研究结果表明, 3种常绿植物冬季光抑制程度与植物的耐冷性呈负相关关系, 且主要决定于阳生叶对冬季低温强光的耐性; 耐冷性强的植物在越冬期具有相对较强的热耗散和CEF-PSI光保护途径, 并能维持PSII和PSI功能的协同性。

关键词: 常绿阔叶植物, 冬季光抑制, 光保护机制, 低温强光, 亚热带

Abstract:

Aims Imbalance between light energy absorption and utilization causes winter photoinhibition in overwintering evergreens. Many studies have investigated the overwintering photoprotective strategies of temperate and boreal evergreens under freezing temperatures. However, little is known about the photoprotective mechanisms of evergreen broadleaf plants in response to low temperatures dominated by above 0 °C in the subtropical winter. This research aims to explore the photoprotective strategies of overwintering evergreen broadleaf species with different cold tolerances in the subtropical region.

Methods This study was carried out on the campus of Jinggangshan University from October 2022 to March 2023. Three evergreen broadleaf species, Photinia × fraseri (high cold resistance), Magnolia grandiflora(moderate cold resistance), and Ficus concinna (cold sensitive), which were planted more than 10 years ago, were selected. The chlorophyll fluorescence parameters of shade leaves and sun leaves were measured from the Detached leaves using Dual-PAM-100/F.

Important findings The winter photoinhibition (WPI) of photosystem II (PSII) and photosystem I (PSI), as well as the photoprotective mechanisms in shade- and sun-leaves of the three evergreen broadleaf species, displayed distinct temperature response characteristics in relation to low temperatures in winter and warming in early spring. During winter, low temperatures combined with strong light only induced slight reversible photoinhibition of PSII in sun leaves of P. × fraseri, but led to severe photoinhibition of both PSII and PSI in sun leaves of M. grandiflora and F. concinna. Furthermore, the reductions in the maximum photochemical efficiency of PSII (F_v/F_m) and the maximum fluorescence signal of P700 reaction center (P_m) in F. concinna were significantly greater than those in M. grandiflora. Low temperatures combined with strong light triggered increases in heat dissipation (NPQ) and cyclic electron flow around PSI (CEF-PSI) to safeguard PSII and PSI of the sun leaves on P. × fraseri during winter. Moreover, low temperature combined with strong light stimulated the compensatory recovery of PSII and PSI functions in sun leaves of P. × fraseri, as manifested by the photochemical quenching (q_P), and the effective quantum yields of PSII and PSI (Y(II) and Y(I)) recovering to a higher level in the warming condition of early spring (March 2023) compared to those in Autumn (October 2022). The functions of PSII and PSI in sun leaves of M. grandiflora continuously declined during winter, but it adopted a photoprotective mechanism of enhancing CEF-PSI and maintaining a relatively strong heat dissipation capacity to maintain the coordination of PSII and PSI functions. Although CEF-PSI was enhanced, the heat dissipation capacity decreased significantly in sun leaves of F. concinna during winter, and low temperatures combined with strong light caused severe damage to PSII and PSI. Low temperatures did not cause obvious photoinhibition damage to shade leaves of the three evergreen species in the subtropical region during winter. Slight reversible photoinhibition of PSI was observed in shade leaves of P. × fraseriand M. grandiflora during winter. Photinia × fraseri possessed the photoprotective mechanism of maintaining a relatively high photochemical capacity and partially closing the PSII reaction center to reduce light absorption, while M. grandiflora mainly adopted the photoprotective mechanism of enhancing CEF-PSI and heat dissipation capacity. Although low temperatures reduced the heat dissipation capacity of shade leaves of F. concinna, the functions of PSII and PSI were not significantly affected, and slight reversible photoinhibition of PSII and PSI was caused in shade leaves of F. concinna during winter. The results indicated that the degree of WPI was negatively correlated with the cold tolerance of the three evergreen broadleaf species, and it was mainly determined by the tolerance of sun leaves to low temperature with strong light in winter in subtropical region. Evergreen broadleaf plants with high cold tolerance possessed relatively strong capacities of heat dissipation and CEF-PSI, and were able to maintain the coordination of PSII and PSI functions during winter.

Key words: evergreen broadleaf plant, winter photoinhibition, photoprotective mechanism, low temperature combined with strong light, subtropical region

闫小红, 胡文海. 亚热带地区3种常绿阔叶植物冬季光保护机制的差异. 植物生态学报, 2025, 49(6): 952-964. DOI: 10.17521/cjpe.2024.0258

YAN Xiao-Hong, HU Wen-Hai. Differences in photoprotective mechanisms during winter in three evergreen broadleaf species in subtropical region. Chinese Journal of Plant Ecology, 2025, 49(6): 952-964. DOI: 10.17521/cjpe.2024.0258

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链接本文: https://www.plant-ecology.com/CN/10.17521/cjpe.2024.0258

https://www.plant-ecology.com/CN/Y2025/V49/I6/952

图/表 8

图1 实验期间日最高气温与最低气温的变化。箭头所指黑框代表测量时间点。

Fig. 1 Changes in daily maximum and minimum air temperature during experimental period. The black boxes pointed by the arrow indicate the time of measurement.

图2 越冬期3种常绿阔叶植物光系统II最大光化学效率(Fv/Fm)和光系统I反应中心P700最大荧光信号(Pm)的变化(平均值±标准误, n = 5)。柱状图上方不同小写字母表示两者间在0.05水平上差异显著。

Fig. 2 Changes in the maximum quantum yield of photosystem II (Fv/Fm) and the maximum fluorescence signal of the P700 reaction center (Pm) in the three evergreen broadleaf species during overwintering (mean ± SE, n = 5). The bars with different lowercase letters indicate significant difference between treatments (p < 0.05).

图3 越冬期3种常绿阔叶植物通过光系统II和光系统I的电子传递速率(ETR)快速光曲线(平均值±标准误, n = 5)。PAR, 光合有效辐射。

Fig. 3 Rapid light curves of electron transport rate (ETR) of photosystem II and photosystem I in the three evergreen broadleaf species during overwintering (mean ± SE, n = 5). PAR, photosynthetically active radiation; SH, shade-leaf; SU, sun-leaf.

表1 越冬期3种常绿阔叶植物通过光系统II和光系统I的最大光合电子流(Jmax)和饱和光强(PARsat) (平均值±标准误, n = 5)

Table 1 The maximum photosynthetic electron flow (Jmax) and saturated irradiance (PARsat) of photosystem II and photosystem I in the three evergreen broadleaf species during overwintering (mean ± SE, n = 5)

参数 Parameter	种类 Species	阴生叶 Shade-leaf			阳生叶 Sun-leaf
参数 Parameter	种类 Species	秋季 Autumn	冬季 Winter	春季 Spring	秋季 Autumn	冬季 Winter	春季 Spring
J_{max-ETR(II) (}μmol·m^-2·s^-1₎	红叶石楠 P. × fraseri	46.6 ± 6.7^Ac	36.6 ± 5.7^Acd	38.0 ± 2.4^Acd	64.9 ± 3.4^Ab	27.6 ± 1.0^Ad	98.8 ± 3.6^Aa
	荷花木兰 M. grandiflora	40.4 ± 4.0^Aa	25.7 ± 3.9^ABb	11.7 ± 1.0^Cc	38.7 ± 2.0^Ba	10.9 ± 2.9^Bc	7.3 ± 0.8^Cc
	雅榕 F. concinna	26.4 ± 2.7^Bb	18.3 ± 1.5^Bc	21.4 ± 1.1^Bbc	43.0 ± 2.1^Ba	3.2 ± 0.9^Cd	18.8 ± 2.1^Bc
J_{max-ETR(I) (}μmol·m^-2·s^-1₎	红叶石楠 P. × fraseri	77.5 ± 7.9^Ac	57.1 ± 6.3^Ad	63.1 ± 3.1^Acd	107.6 ± 6.2^Ab	48.4 ± 1.3^Ad	177.4 ± 6.1^Aa
	荷花木兰 M. grandiflora	73.3 ± 6.9^Aa	44.2 ± 5.1^ABb	23.9 ± 1.4^Cc	73.6 ± 4.6^Ba	27.3 ± 4.0^Bc	19.1 ± 2.2^Cc
	雅榕 F. concinna	48.7 ± 2.1^Bbc	41.3 ± 2.2^Bbc	50.1 ± 3.0^Bb	82.3 ± 3.9^Ba	25.5 ± 2.5^Bd	39.7 ± 5.1^Bc
PAR_{max-ETR(II) (}μmol·m^-2·s^-1₎	红叶石楠 P. × fraseri	703 ± 53^Acd	750 ± 83^Abc	648 ± 41^Acd	871 ± 26^Ab	577 ± 15^Ad	1 343 ± 47^Aa
	荷花木兰 M. grandiflora	646 ± 57^Aa	473 ± 30^Bb	263 ± 16^Bc	672 ± 62^Aa	390 ± 49^Bbc	265 ± 39^Cc
	雅榕 F. concinna	576 ± 20^Ab	542 ± 21^Bb	706 ± 122^Aab	866 ± 138^Aa	237 ± 21^Cc	599 ± 124^Bab
PAR_{max-ETR(I) (}μmol·m^-2·s^-1₎	红叶石楠 P. × fraseri	1 030 ± 8^Abc	857 ± 68^Acd	1 200 ± 147^Aab	1 037 ± 57^Ab	696 ± 32^Ad	1 290 ± 35^Aa
	荷花木兰 M. grandiflora	1 083 ± 47^Aa	731 ± 80^Ac	344 ± 26^Bde	891 ± 43^Ab	417 ± 34^Bd	241 ± 42^Ce
	雅榕 F. concinna	787 ± 54^Bb	675 ± 38^Ab	1 118 ± 178^Aa	906 ± 52^Aab	299 ± 35^Cc	493 ± 28^Bc

表1 越冬期3种常绿阔叶植物通过光系统II和光系统I的最大光合电子流(Jmax)和饱和光强(PARsat) (平均值±标准误, n = 5)

参数 Parameter	种类 Species	阴生叶 Shade-leaf			阳生叶 Sun-leaf
参数 Parameter	种类 Species	秋季 Autumn	冬季 Winter	春季 Spring	秋季 Autumn	冬季 Winter	春季 Spring
J_{max-ETR(II) (}μmol·m^-2·s^-1₎	红叶石楠 P. × fraseri	46.6 ± 6.7^Ac	36.6 ± 5.7^Acd	38.0 ± 2.4^Acd	64.9 ± 3.4^Ab	27.6 ± 1.0^Ad	98.8 ± 3.6^Aa
	荷花木兰 M. grandiflora	40.4 ± 4.0^Aa	25.7 ± 3.9^ABb	11.7 ± 1.0^Cc	38.7 ± 2.0^Ba	10.9 ± 2.9^Bc	7.3 ± 0.8^Cc
	雅榕 F. concinna	26.4 ± 2.7^Bb	18.3 ± 1.5^Bc	21.4 ± 1.1^Bbc	43.0 ± 2.1^Ba	3.2 ± 0.9^Cd	18.8 ± 2.1^Bc
J_{max-ETR(I) (}μmol·m^-2·s^-1₎	红叶石楠 P. × fraseri	77.5 ± 7.9^Ac	57.1 ± 6.3^Ad	63.1 ± 3.1^Acd	107.6 ± 6.2^Ab	48.4 ± 1.3^Ad	177.4 ± 6.1^Aa
	荷花木兰 M. grandiflora	73.3 ± 6.9^Aa	44.2 ± 5.1^ABb	23.9 ± 1.4^Cc	73.6 ± 4.6^Ba	27.3 ± 4.0^Bc	19.1 ± 2.2^Cc
	雅榕 F. concinna	48.7 ± 2.1^Bbc	41.3 ± 2.2^Bbc	50.1 ± 3.0^Bb	82.3 ± 3.9^Ba	25.5 ± 2.5^Bd	39.7 ± 5.1^Bc
PAR_{max-ETR(II) (}μmol·m^-2·s^-1₎	红叶石楠 P. × fraseri	703 ± 53^Acd	750 ± 83^Abc	648 ± 41^Acd	871 ± 26^Ab	577 ± 15^Ad	1 343 ± 47^Aa
	荷花木兰 M. grandiflora	646 ± 57^Aa	473 ± 30^Bb	263 ± 16^Bc	672 ± 62^Aa	390 ± 49^Bbc	265 ± 39^Cc
	雅榕 F. concinna	576 ± 20^Ab	542 ± 21^Bb	706 ± 122^Aab	866 ± 138^Aa	237 ± 21^Cc	599 ± 124^Bab
PAR_{max-ETR(I) (}μmol·m^-2·s^-1₎	红叶石楠 P. × fraseri	1 030 ± 8^Abc	857 ± 68^Acd	1 200 ± 147^Aab	1 037 ± 57^Ab	696 ± 32^Ad	1 290 ± 35^Aa
	荷花木兰 M. grandiflora	1 083 ± 47^Aa	731 ± 80^Ac	344 ± 26^Bde	891 ± 43^Ab	417 ± 34^Bd	241 ± 42^Ce
	雅榕 F. concinna	787 ± 54^Bb	675 ± 38^Ab	1 118 ± 178^Aa	906 ± 52^Aab	299 ± 35^Cc	493 ± 28^Bc

表2 光环境和季节变化对3种常绿阔叶植物最大光合电子流(Jmax)和饱和光强(PARsat)的影响

Table 2 Influences of light environment and season variation on the maximum photosynthetic electron flow (Jmax) and saturated irradiance (PARsat) of three evergreen broadleaf plants

参数 Parameters	F
参数 Parameters	光环境 Light (L)	季节 Season (S)	光环境×季节 L × S
红叶石楠 Photinia × fraseri
J_max-ETR(II)	45.552^***	37.758^***	34.486^***
PAR_sat-ETR(II)	32.514^***	23.160^***	39.240^***
J_max-ETR(I)	97.833^***	73.389^***	62.978^***
PAR_sat-ETR(I)	0.131	20.772^***	1.546
荷花木兰 Magnolia grandiflora
J_max-ETR(II)	9.766^**	63.541^***	3.157
PAR_sat-ETR(II)	0.248	38.768^***	0.821
J_max-ETR(I)	3.890	73.700^***	2.000
PAR_sat-ETR(I)	26.515^***	104.589^***	2.386
雅榕 Ficus concinna
J_max-ETR(II)	0.067	87.579^***	38.051^***
PAR_sat-ETR(II)	0.301	7.249^**	5.450^*
J_max-ETR(I)	0.855	48.547^***	33.699^***
PAR_sat-ETR(I)	18.953^***	11.339^***	10.526^***

图4 越冬期3种常绿阔叶植物光化学猝灭(qP)、非光化学猝灭(NPQ)和围绕光系统I的环式电子传递(CEF-PSI)的变化(平均值±标准误, n = 5)。柱状图上方不同小写字母表示两者间在0.05水平上差异显著。

Fig. 4 Changes in the photochemical quenching (qP), non-photochemical quenching (NPQ), and the cyclic electron flow around photosystem I (CEF-PSI) in the three evergreen broadleaf species during overwintering (mean ± SE, n = 5). The bars with different lowercase letters indicate significant difference between treatments (p < 0.05).

图5 越冬期3种常绿阔叶植物光系统II (PSII)能量分配的变化(平均值±标准误, n = 5)。Y(II), PSII实际光化学量子产量; Y(NO), PSII非调节性能量耗散的量子产量; Y(NPQ), PSII调节性能量耗散的量子产量。柱状图上方不同小写字母表示两者间在0.05水平上差异显著。

Fig. 5 Changes in the energy partitioning of photosystem II (PSII) in the three evergreen broadleaf species during overwintering (mean ± SE, n = 5). Y(II), effective PSII quantum; Y(NO), quantum yield of nonregulation energy dissipation; Y(NPQ), quantum yield of regulated energy dissipation. The bars with different lowercase letters indicate significant difference between treatments (p < 0.05).

图6 越冬期3种常绿阔叶植物光系统I (PSI)能量分配的变化(平均值±标准误, n = 5)。Y(I), PSI光化学量子产量; Y(NA), PSI受体侧限制引起的非光化学量子产量; Y(ND), PSI供体侧限制引起的热耗散量子产量。柱状图上方不同小写字母表示两者间在0.05水平上差异显著。

Fig. 6 Changes in the energy partitioning of photosystem I (PSI) in the three evergreen broadleaf species during overwintering (mean ± SE, n = 5). Y(I), effective quantum yield of PSI; Y(NA), quantum yield of PSI non-photochemical energy dissipation due to acceptor; Y(ND), heat dissipation efficiency at the donors quantum yield of PSI. The bars with different lowercase letters indicate significant difference between treatments (p < 0.05).

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