低温胁迫下链霉菌TOR3209对番茄叶绿素荧光特性和叶黄素循环的影响

doi:10.3864/j.issn.0578-1752.2024.22.011

Abstract

Abstract:

【Objective】In order to explore the biological mechanism of Streptomyces sp. TOR3209 in improving the low temperature tolerance of tomato, and to reveal the protective mechanism of TOR3209 on photosystem II (PSII) from two aspects (chlorophyll fluorescence characteristics and xanthophyll cycle).【Method】As the experimental material, tomato seedlings of quadrifoil stage were applied with TOR3209 when transplanted into the pots, cold stress (5 ℃) was imposed on the 30th day after transplanting. The experiment was divided into four parts, which were inoculated plants (TOR3209), non-inoculated plants (NI), inoculated plants exposed to cold stress (TOR3209+C) and non-inoculated plants exposed to cold stress (NI+C). The differences in PSII performance, chlorophyll fluorescence parameters related to NPQ, xanthophyll cycle component, violaxanthin de-epoxidase (VDE) activity, and ascorbate-glutathione (AsA-GSH) cycle in plants of different treatments were compared.【Result】Streptomyces sp. TOR3209 could alleviate the decrease of actual photochemical efficiency of PSII Y (II) by cold stress and avoid PSII photoinhibition. Defensing to the cold stress, the shape of chlorophyll a fluorescence transient (OJIP) curve was significantly changed with increased in J step and an emergence of K step; while the approximated initial slope of the fluorescence transient (M_o) increased, and the rate at which trapped excitons transfer electrons to other electron receptors downstream of primary quinone receptor (Q_A) in the electron transport chain (Ψ_o) decreased, and the performance index on absorption basis (PI_ABS) decreased in JIP-test of tomato leaves. The inoculation of TOR3209 under cold stress prevented a significant increase in variable fluorescence intensity at J step and an emergence of K step, while the M_o, Ψ_oand PI_ABSreturned to the levels in plants of NI, indicating that TOR3209 protected the electron transporters at PSII acceptor side and oxygen-evolving complex (OEC) at PSII donor side. The inoculation of TOR3209 also prevented a significant decrease in PI_ABS and the performance index on cross section basis (PI_CS) in tomato leaves as revealed by JIP-test, which in combination with the significantly increased NPQ and protective heat dissipation (Ф_NPQ), as well as the significantly decreased non-regulatory energy dissipation (Ф_NO), evidenced that the main mechanism of TOR3209 to protect PSII was the protective heat dissipation. Cold stress apparently decreased the de-epoxidation state (DEPS) of xanthophyll cycle, at the same time, reduced the levels of xanthophyll cycle components, the activities of VDE and antioxidases in AsA-GSH pathway (ascorbate peroxidase APX, glutathione reductase GR, monodehydroascorbate reductase MDHAR), and contents of antioxidants (ascorbate AsA, glutathione GSH), slowed down the xanthophyll cycle, and depressed the photosynthetic capacity of tomato leaves. However, TOR3209 inoculation could increase the DEPS of xanthophyll cycle, enhance the levels of xanthophyll cycle components and VDE activity under cold stress, which further raised the level of PSII non-photochemical fluorescence quenching coefficient, prevented excess excitation energy, and protected the photosynthetic apparatus. Meanwhile, TOR3209 inoculation improved the activities of the above-mentioned antioxidases and AsA content under cold stress, optimized the AsA-GSH cycle to confront the accumulation of reactive oxygen species (ROS) and facilitate xanthophyll cycle.【Conclusion】The improvement of cold tolerant capacity in tomato plants by TOR3209 inoculation was reflected in maintaining PSII stability by increasing the photosynthetic electron transfer activity, alleviating the damage of PSII photoinhibition via enhancing the xanthophyll cycle, and reducing oxidative stress on PSII by optimizing AsA-GSH cycle.

Key words: tomato (Solanum lycopersicum), Streptomyces, cold stress, PSII photoinhibition, chlorophyll fluorescence, xanthophyll cycle

MA Jia, PENG JieLi, JIA Nan, WANG Xu, WANG ZhanWu, HU Dong. Effects of Streptomyces sp. TOR3209 on Chlorophyll Fluorescence Characteristics and Xanthophyll Cycle in Tomato Plants Under Cold Stress[J].Scientia Agricultura Sinica, 2024, 57(22): 4522-4540.

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Figures/Tables 13

Table 1

Definition of fluorescence parameters and formulas used in JIP-test analysis"

参数及公式Parameter and formula	注释Definition
F_o	最小荧光强度Minimal recorded fluorescence intensity
F_m	最大荧光强度Maximal recorded fluorescence intensity
V_J=(F_J-F_o)/(F_m-F_o)	J点的相对可变荧光强度Relative variable fluorescence intensity at the J-step
M_o=4×(F_{300 μs}-F_o)/(F_m-F_o)	相对荧光曲线的初始斜率Approximated initial slope of the fluorescence transient
ABS/RC=M_o×(1/V_J)×(1/φ_Po)	单位反应中心吸收的光能Absorption flux per reaction center
TR_o/RC=M_o×(1/V_J)	单位反应中心捕获的光能Trapped energy flux per reaction center
ET_o/RC=M_o×(1/V_J)×ψ_o	单位反应中心捕获的用于电子传递的能量（在t=0时）Electron transport flux per reaction center (at t=0)
DI_o/RC=(ABS/RC)-(TR_o/RC)	单位反应中心耗散的能量（在t=0时）Dissipated energy flux per reaction center (at t=0)
φ_Po=TR_o/ABS	最大光化学效率（在t=0时）Maximum quantum yield for primary photochemistry (at t=0)
Ψ_o=ET_o/TR_o	捕获的激子将电子传递到电子传递链中超过Q_A的其他电子受体的概率（在t=0时） Probability that a trapped exciton moves an electron into the electron transport chain beyond Q_A (at t=0)
φ_Eo=ET_o/ABS	电子传递的量子产额（在t=0时）Quantum yield for electron transport (at t=0)
φ_Do=1-φ_Po	用于热耗散的量子比率（在t=0时）Quantum ratio for dissipated energy (at t=0)
ABS/CS_o≈F_o	单位横截面积吸收的光能（在t=0时）Absorption flux per cross-sectional area (at t=0)
TR_o/CS_o=φ_Po×(ABS/CS_o)	单位横截面积捕获的光能（在t=0时）Trapped energy flux per cross-sectional area (at t=0)
ET_o/CS_o=φ_Eo×(ABS/CS_o)	单位横截面积电子传递的量子产额（在t=0时） Quantum yield for electron transport flux per cross-sectional area (at t=0)
DI_o/CS_o=(ABS/CS_o)-(TR_o/CS_o)	单位横截面积的热耗散能量（在t=0时）Dissipated energy flux per cross-sectional area (at t=0)
RC/CS_o=φ_Po×(V_J/M_o)×(ABS/CS_o)	单位面积有活性反应中心的数量Number of reaction centers per unit area
PI_ABS=(RC/ABS)×[φ_Po/(1-φ_Po)]×[Ψ_o/(1-Ψ_o)]	以吸收光能为基础的性能指数Performance index on absorption basis
PI_CS=(RC/CS_o)×[φ_Po/(1-φ_Po)]×[Ψ_o/(1-Ψ_o)]	以单位面积为基础的性能指数（在t=0时）Performance index on cross section basis (at t=0)

Table 1

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叶黄素循环 Xanthophyll cycle	处理 Treatment	0 d	1 d	3 d	6 d	10 d
总叶黄素 Total xanthophyll (mmol·mol^-1 Chl)	TOR3209+C	111.77±4.15a	81.41±2.64ab	109.82±4.46a	79.66±5.30ab	76.05±10.87ab
	NI+C	86.36±19.24a	67.64±5.15b	69.91±10.00b	63.52±7.64b	62.81±4.93b
	TOR3209	111.77±4.15a	92.65±12.30a	109.43±17.44a	98.33±5.46a	89.84±2.18a
	NI	86.36±19.24a	79.11±10.14ab	77.46±13.24b	73.04±22.03b	83.84±7.44a
叶黄素脱环氧化状态DEPS	TOR3209+C	70.96±7.05a	74.94±2.49a	80.32±3.72a	89.13±1.48a	91.26±0.40a
	NI+C	63.79±8.78a	70.15±3.11ab	77.11±4.04ab	82.31±1.78a	85.86±2.37b
	TOR3209	70.96±7.05a	74.56±4.04a	73.85±1.95bc	71.30±4.65b	70.08±2.22c
	NI	63.79±8.78a	66.30±4.49b	70.75±2.54c	68.29±7.46b	65.50±2.26d

处理 Treatment	VDE活性VDE activity (μmol·min^-1·g^-1)
处理 Treatment	0 d	1 d	3 d	6 d	10 d
TOR3209+C	3.00±0.07a	3.58±0.03a	3.11±0.09a	3.60±0.03a	3.28±0.09a
NI+C	2.90±0.10a	2.10±0.10d	1.56±0.07d	1.68±0.05d	1.69±0.09d
TOR3209	3.00±0.07a	2.96±0.08b	2.72±0.14b	2.75±0.01b	3.08±0.05b
NI	2.90±0.10a	2.40±0.07c	2.21±0.10c	1.83±0.08c	2.56±0.03c

抗氧化剂 Antioxidant	处理 Treatment	0 d	1 d	3 d	6 d	10 d
抗坏血酸 AsA	含量Content (μg·g^-1)
	TOR3209+C	391.26±127.99a	443.84±64.03c	572.45±101.04b	461.70±55.45ab	293.58±90.89c
	NI+C	362.86±90.38a	363.85±30.57c	395.99±47.24c	388.44±33.12b	283.26±94.51c
	TOR3209	391.26±127.99a	827.13±42.62a	819.71±35.95a	520.25±82.13a	602.01±42.44a
	NI	362.86±90.38a	687.80±28.62b	628.16±64.83b	485.52±36.93ab	461.76±56.24b
	F值F value
	T	ns	18.119**	22.651**	ns	ns
	C	ns	196.438***	38.447***	5.939*	32.101***
	T×C	ns	ns	ns	ns	ns
还原型谷胱甘肽 GSH	含量Content (μmol·g^-1)
	TOR3209+C	0.48±0.10a	0.49±0.09b	0.61±0.08ab	0.83±0.03b	0.60±0.09c
	NI+C	0.44±0.09a	0.47±0.12b	0.55±0.04b	0.82±0.17b	0.53±0.06c
	TOR3209	0.48±0.10a	0.88±0.09a	0.75±0.10a	1.77±0.08a	1.72±0.12a
	NI	0.44±0.09a	0.54±0.10b	0.69±0.09ab	1.08±0.22b	1.02±0.08b
	F值F value
	T	ns	9.542*	ns	16.968**	53.589***
	C	ns	14.994**	8.396*	49.793***	232.974***
	T×C	ns	7.099*	ns	16.350**	35.053***

抗氧化酶 Antioxidase	处理 Treatment	0 d	1 d	3 d	6 d	10 d
抗坏血酸过氧化物酶 APX	酶活性Enzyme activity (nmol·min^-1·g^-1)
	TOR3209+C	664.38±8.71a	386.95±9.57b	227.79±6.31c	517.68±42.28c	248.32±43.18c
	NI+C	422.43±35.46b	227.15±20.83c	127.61±19.59d	219.01±13.23d	252.45±27.61c
	TOR3209	664.38±8.71a	542.77±33.78a	947.39±54.25a	969.51±24.93a	519.76±27.57a
	NI	422.43±35.46b	507.89±12.78a	402.39±13.43b	611.92±23.67b	331.44±20.41b
	F值F value
	T	263.408***	62.140***	352.071***	410.892***	26.757**
	C	ns	312.452***	836.310***	680.805***	96.849***
	T×C	ns	25.586**	167.349***	ns	29.211**
谷胱甘肽还原酶 GR	酶活性Enzyme activity (U·g^-1)
	TOR3209+C	638.41±78.70a	508.06±32.07ab	418.70±20.40b	291.26±22.55b	491.78±47.88a
	NI+C	404.28±48.16b	466.47±62.81b	176.15±35.84c	258.16±55.02b	342.97±59.97b
	TOR3209	638.41±78.70a	595.77±51.74a	614.98±52.69a	590.94±89.21a	563.92±95.40a
	NI	404.28±48.16b	584.72±51.32a	548.91±88.40a	533.82±92.16a	505.00±6.97a
	F值F value
	T	38.632***	ns	23.248**	ns	8.608*
	C	ns	12.373**	79.035***	49.680***	10.940*
	T×C	ns	ns	7.602*	ns	ns
单脱氢抗坏血酸还原酶 MDHAR	酶活性Enzyme activity (nmol·min^-1·g^-1)
	TOR3209+C	108.54±24.98a	101.16±46.02ab	81.88±11.51a	119.43±18.93a	104.10±18.42a
	NI+C	56.38±16.37b	44.77±2.42b	45.43±10.95b	73.52±8.65ab	63.63±10.29ab
	TOR3209	108.54±24.98a	116.62±40.55a	63.69±8.57ab	79.40±37.78ab	107.44±44.15a
	NI	56.38±16.37b	70.41±16.08ab	48.74±9.62b	60.62±21.43b	44.43±5.93b
	F值F value
	T	18.297**	7.841*	18.949**	5.411*	13.221**
	C	ns	ns	ns	ns	ns
	T×C	ns	ns	ns	ns	ns

Effects of Streptomyces sp. TOR3209 on Chlorophyll Fluorescence Characteristics and Xanthophyll Cycle in Tomato Plants Under Cold Stress

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