Improving Plant Growth and Alleviating Photosynthetic Inhibition and Oxidative Stress From Low-Light Stress With Exogenous GR24 in Tomato (Solanum lycopersicum L.) Seedlings

Abstract

Low light (LL) is one of the main limiting factors that negatively affect tomato growth and yield. Techniques of chemical regulation are effective horticultural methods to improve stress resistance. Strigolactones (SLs), newly discovered phytohormones, are considered as important regulators of physiological responses. We investigated the effects of foliage spray of GR24, a synthesized SLs, on tomato seedlings grown under LL stress conditions. The results showed that application of GR24 effectively mitigated the inhibition of plant growth and increased the fresh and dry weight of tomato plants under LL. Additionally, GR24 also increased the chlorophyll content (Chla and Chlb), the net photosynthetic rate (Pn), the photochemical efficiency of photosystem (PS) II (Fv/Fm), and the effective quantum yield of PSII and I [Y(II) and Y(I)], but decreased the excitation pressure of PSII (1-qP), the non-regulatory quantum yield of energy dissipation [Y(NO)] and the donor side limitation of PSI [Y(ND)] under LL. Moreover, application of GR24 to LL-stressed tomato leaves increased the electron transport rate of PSII and PSI [ETR(II) and ETR(I)], the ratio of the quantum yield of cyclic electron flow (CEF) to Y(II) [Y(CEF)/Y(II)], the oxidized plastoquinone (PQ) pool size and the non-photochemical quenching. Besides, GR24 application increased the activity and gene expression of antioxidant enzymes, but it reduced malonaldehyde (MDA) and hydrogen peroxide (H₂O₂) content in LL-stressed plants. These results suggest that exogenous application of GR24 enhances plant tolerance to LL by promoting plant utilization of light energy to alleviate the photosystem injuries induced by excess light energy and ROS, and enhancing photosynthesis efficiency to improve plant growth.

Keywords: endogenous GR24; low light; photoinhibition; photosynthesis; tomato.

Figure 1

Effects of exogenous GR24 on the net photosynthetic rate (A) and PSII activity (B) of tomato leaves under LL stress. Data are the means of four replicates with standard errors shown by vertical bars. ^∗ and ^∗∗ indicate statistically significant differences at P ≤ 0.05 and P ≤ 0.01, respectively. Multiple comparisons between the figures among the treatments under LL are shown in parentheses.

Figure 2

Effects of exogenous GR24 on Fv′/Fm′ and 1-qP of tomato leaves under LL stress on the 7^th day of treatment. Fv′/Fm′, efficiency of excitation capture by open PSII centers; 1-qP, excitation pressure of PSII. Lowercase and capital letters represent significant differences between treatments at P ≤ 0.05 and P ≤ 0.01 by the LSD test, respectively.

Figure 3

Effects of exogenous GR24 on intersystem energy distribution and electron transport rate (ETR) of tomato seedlings under LL stress. Y(II), effective quantum yield of PSII (A); Y(NO), fraction of energy that is passively dissipated in form of heat and fluorescence (B); Y(NPQ), fraction of energy dissipated in form of heat via the regulated non-photochemical quenching mechanism (C); ETR(II), ETR of PSII (D); Y(I), effective quantum yield of PSI (E); Y(ND), fraction of overall P700 that is oxidized in a given state (F); Y(NA), fraction of overall P700 that cannot be oxidized in a given state (G); ETR(I), ETR of PS I (H). ^∗ and ^∗∗ indicate statistically significant differences at P ≤ 0.05 and P ≤ 0.01, respectively. Multiple comparisons between the figures among the treatments under LL are shown in parentheses.

Figure 4

Effects of exogenous GR24 on the expression of genes encoding the PSII and PSI reaction center core proteins of tomato seedlings under LL stress. Expression levels of the corresponding genes at day 0 were used as control. RT-PCR was conducted with three replications. ^∗ Indicate statistically significant differences at P ≤ 0.05. Multiple comparisons between the figures among the treatments under LL are shown in parentheses. (A) The expression of psbA; (B) the expression of psbB; (C) the expression of psbC; (D) the expression of psbD; (E) the expression of psbP; (F) the expression of cab; (G) the expression of psaA; (H) the expression of psaB.

Figure 5

Effects of exogenous GR24 on rETR-PAR response curve and fitting parameters of tomato seedlings under LL stress on the 7^th day of treatment. Curves were fitted with OriginLab software, and the fitting parameters were determined by Dual-PAM measuring software, as shown in the embedded tables. The fitted curves are displayed as dotted lines. Fitted equation: rETR = rETR_max ⋅ E_k ⋅ (α ⋅ PAR/rETR_max); rETR, relative electron transport rate; rETR_max, maximum potential relative electron transport rate; α, the initial slope of the rapid light curve; E_k, semi-light saturation point. (A) The rETR(II) light response curve and fitting parameters, (B) the rETR(I) light response curve and fitting parameters.

Figure 6

Effects of exogenous GR24 on the performance of rapid induction kinetics (A) and JIP-test analysis (B) of tomato seedlings under LL stress on the 7^th day of treatment. PI(abs), performance index based on the absorption of light energy; ABS/RC, average absorption per active RC; TRo/RC, flux of exciton trapped per active RC; ETo/RC, electron transport per active RC; DIo/RC, ratio of total dissipation to the amount of active RC; φPo, maximum yield of primary photochemistry; φo, the efficiency to conserve trapped excitation energy as redox energy; φEo, quantum yield of absorbed photons for electron transport; φRo, quantum yield of reduction of final electron acceptors of PSI per photon absorbed; φDo, quantum yield of heat dissipation.

Figure 7

Effects of exogenous GR24 on the activity of SOD (A), CAT (B), POD (C), and the transcript level of sod1 (D), cat1 (E), and cevi16 (F) in tomato leaves under LL stress. The transcript level shown in the figure are from the 7^th day of treatment. ^∗ and ^∗∗ indicate statistically significant differences at P ≤ 0.05 and P ≤ 0.01, respectively. Multiple comparisons between the figures among the treatments under LL are shown in parentheses. Lowercase letters represent significant differences difference between treatments at P ≤ 0.05 by the LSD test.