Background

Tomato (Solanum lycopersicum) is one of the most important vegetable crops from Solanaceae (Mccormick et al., 1986). However, the yield and quality of tomato were affected by a variety of abiotic stresses when they were in a complex environment (Hichri et al., 2014; Shi et al., 2014). Drought stress is the major problem for agriculture because its adverse environmental factors prevent plants from realizing their full genetic potential (Zhu, 2002). Plants are often through the changes of external morphology, photosynthetic mechanism, osmotic adjustment, antioxidant enzymes and other aspects to adapt or resist water stress of the environment. In drought stress, the main reason of the plant photosynthesis decrease is the chloroplast dysfunction, but stomatal limitation. The photosynthesis metabolism is an important metabolic process in plants, and has become an important content in the study of plant physiology and ecology of plants because of its stability, it can be used to judge the plant growth and stress resistance index (Taiz and Zeiger, 2010). Drought stress reduced chlorophyll content, decreased the effective area of photosynthesis, and even destroyed the photosynthetic mechanism of plants, resulting in changes in chlorophyll fluorescence parameters and finally affected the normal life activities of crops (Aroca et al., 2003; NR and E, 2004).

The chlorophyll fluorescence kinetic technique can rapidly and sensitively reflect the photosynthetic system II (PS II) without damage in plant. Compared with the gas exchange index of plant leaves, chlorophyll fluorescence parameters reflect the intrinsic characteristics of the absorption, transmission, dissipation and distribution of light energy in plant (Krause and Weis, 1984). In this paper, tomato seedlings were treated for 3, 6, 12 or 24 h by polyethylene glycol 6000 (PEG 6000) to simulate the drought stress. The effects of drought stress on chlorophyll fluorescence characteristics of tomato leaves and the characteristics of Chlorophyll fluorescence parameters were analyzed by IMAGING-PAM modulated chlorophyll fluorescence in order to provide theoretical basis for tomato cultivation and breeding.

1 Result

The results confirm the possibility of the photosynthesis inhibition of tomato seedlings by drought stress (Xu et al., 2011). The parameters of chlorophyll fluorescence induction were nearly equal in parallel control group of tomato cultivars.

1.1 Effects of drought stress on Fm in leaves of tomato seedlings

Fm is the fluorescence yield in a fully closed state of PSII reaction center, reflects the circumstances of electron transfer of PSII (XB and TC, 1988). Figure 1 shows, the FM value of tomato seedlings after drought treatment was significantly lower than that without drought treatment, treatment time was 0 hours. As a whole, the FM value declined by 9.7%, indicating that the drought treatment of 15% PEG 6000 simulation reduced the electron transport of PS II and inhibited the photosynthetic carbon metabolism in leaves of tomato seedlings.

Figure 1 Changes of the maximum fluorescence (Fm) of tomato seedlings under drought stress. Each value represents the mean±SE of at least three independent experiments

1.2 Effects of drought stress on Y (II) in leaves of tomato seedlings

PS2 plays an important role in the response of plants to environmental stresses and it is a very sensitive component of the photosynthetic systems (Yordanov et al., 1999; Hassan, 2006). The effective PS-II quantum yield (Y (II)) reflects the primary light harvesting efficiency in the absence of partial PS II reaction centers, under light adaptation conditions. The change in photosynthesis would be reflected ultimately in growth and yield (Hassan, 2006). Figure 2 shows, the value of Y (II) initially increased slightly and then decline eventually leveling off trend with the increasing of drought treatment time. As a whole, the Y (II) value was declined by 43.6%.

Figure 2 Changes of the effective PS-II quantum yield (YII)) of tomato seedlings under drought stress. Each value represents the mean±SE of at least three independent experiments

1.3 Effects of drought stress on ETR in leaves of tomato seedlings

The electron transport rate (ETR) mainly reflects the circumstances of actual electron transport in the PS II reaction center under light adaptation conditions. The results of electron transport rate (ETR) showed that ETR value was lower under drought stress than control check, especially when the drought stress treatment time up to 6 to 12 hours, the ETR value drops sharply, then increased slightly (Figure 3). As a whole, the ETR value was declined by 44.5%.

Figure 3 Changes of the effective PS-II quantum yield ETR of tomato seedlings under drought stress. Each value represents the mean±SE of at least three independent experiments

1.4 Effects of drought stress on qP in leaves of tomato seedlings

Photochemical quenching is defined by fluorescence quenching caused by the inactivation of photosynthesis, which reflects the electron transport activity of PS II and the reduction state of QA. Figure 4 shows that qP decreased from 0.646 to 0.4013 under the drought stress, which reflects the ability of oxidation of QA weakened, namely electron transfer activity of PSII decreased.

Figure 4 Changes of the effective PS-II quantum yield qP of tomato seedlings under drought stress. Each value represents the mean±SE of at least three independent experiments

1.5 Effects of drought stress on qN in leaves of tomato seedlings

The fluorescence quenching caused by thermal dissipation is called non photochemical quenching (qN) (Figure 5). It reflects the ability of plants to dissipate excess energy as thermal energy, that is, a self protective mechanism of plants, can protect the photosynthetic mechanism of plants. As can be seen that 15% PEG 6000 simulated drought stress treatment induced qN increased significantly, reflecting, under drought stress, thermal energy dissipation of PS II increased in tomato seedlings and the part of light energy used in photochemical reaction decreased.

Figure 5 Changes of the effective PS-II quantum yield qN of tomato seedlings under drought stress. Each value represents the mean±SE of at least three independent experiments

2 Discussion

Tomato is one of the most important vegetable crop from Solanaceae (Rai et al., 2013). But the yield and quality of tomato were greatly affected by various abiotic stresses when they were exposed to complex environmental conditions (Hichri et al., 2014; Shi et al., 2014). Our experiments were designed to clarify whether the Chlorophyll fluorescence can as a index to detect a plant’s ability to tolerate drought stress damage and extent to which those stresses damage (Khalekuzzaman et al., 2015; Maxwell and Johnson, 2000). Drought stress drastically affects the photosynthetic efficiency of the tomato resulting in reduced grain yield (Liu et al., 2016; Hauptherting and Fock, 2000).

In this study, the Fm value decreased during drought stress. Fm is the fluorescence yield in a fully closed state of PSII reaction center, reflects the circumstances of electron transfer of PS. The decreased of Fm value indicates that the transport of energy, which was absorbed by the PSII antenna pigments, was reduced used to photochemical reactions, whereas the fluorescence and heat dissipation increased. In the preceding study, the Fm value also decreased in Lycium ruthenicum Murr. seedlings, which suggested that drought stress impacted the openness of PSII reaction centres (Guo et al., 2016). The value of Y (II) initially increased slightly and then decline eventually leveling off trend with the increasing of drought treatment time, which was also reported that the decrease in Y (II) values under drought stress condition in cucumber seedlings in 2008 (Li et al., 2008). Y (II) reflects the primary light harvesting efficiency in the absence of partial PS II reaction centers, under light adaptation conditions. The value of Y (II) decreased indicating the electron supply of photosynthetic carbon metabolism limited, thus the photosynthesis was inhibited. The both of the value of ETR and qP all decreased, the fundamental reason predicted is the drought stress caused fluidity of thylakoid membrane decreased, thus affecting the reaction center of the thylakoid membrane, light harvesting antenna, structure of the electron transfer protein changes, finally the photosynthetic efficiency was affected. The result shows that 15% PEG 6000 mimics drought stress treatment induced qN increased significantly, reflecting, under drought stress, tomatoes are forced to release excessive amounts of energy absorbed by PS II through thermal dissipation, that of tomato seedlings to protect PSII from damage by increasing thermal energy dissipation.

In summary, the photosynthesis of tomato seedlings was more sensitive to drought. It were inhibited that the light harvesting efficiency, photochemical conversion and photosynthetic electron transport under drought stress, which must affect the yield and quality of tomato. In addition, the kinetic parameters of chlorophyll fluorescence in leaves of tomato seedlings were very sensitive to drought stress, can be used as an important means of screening of tomato cultivars tolerant to drought, accelerating the identification and breeding of drought tolerant varieties.

3 Materials and Methods

3.1 Materials

Plant material, Moneymaker comes from tomato Research Institute of Northeast Agricultural University was grown in a growth incubator (photoperiod 14 h, day/night temperature 24/18°C) from October 2016 to January 2017 in plastic pots containing an organic soil watered every 3d at the field capacity. 

3.2 Stress treatments

The tomato seedlings were transferred under open air hydroponics for 48 hours, when they in the raising period of four-leaf stage. Then, the seedlings were exposed to 15% PEG 6000 for drought stress treatments. Young leaves were collected at different time points (0, 3, 6, 12 and 24 h) after treatment. Three biological replicates were performed for each time point.

3.3 Chlorophyll fluorescence measurements

Chlorophyll fluorescence was measured on leaf discs following dark pretreatment for 30 min with IMAGING-PAM chlorophyll fluorometer (WALZ, German). The minimal fluorescence yield (F0) and maximal fluorescence yield (Fm) were measured by applying measuring light source (<0.5 μmol·m^-2·s^-1) and saturating light pulse of 5,000 μmol·m^-2·s^-1 (Soto et al., 2014). Finally we obtained the following parameters: Fm, the effective PSII quantum yield (YII), the photosynthetic electron transport rate (ETR), the photochemical quenching (qP), the non-photochemical quenching (NPQ).

Authors' contributions

Jia Zhang, Junfang Liu is the principal executor of the experiment; Tingting Zhao and Xiangyang Xu are the writers and directors of the article. All the authors have read and agreed to the final text.

Acknowledgments

The authors are grateful to the National Key R&D Progrem of China (2017YFD0101900), the China Agriculture Research System (CARS-23-A-16) and the Science Foundation of Heilongjiang Province (C2017024) for supporting funds to conduct this research work.

References

Aroca R., Irigoyen J.J., and Sánchez-Díaz M., 2003, Drought enhances maize chilling tolerance. II. Photosynthetic traits and protective mechanisms against oxidative stress, Physiologia Plantarum, 117: 540-549

https://doi.org/10.1034/j.1399-3054.2003.00065.x

Guo Y.Y., Yu H.Y., Kong D.S., Yan F., and Zhang Y.J., 2016, Effects of drought stress on growth and chlorophyll fluorescence of Lycium ruthenicum Murr. seedlings, Photosynthetica, 54: 524-531

https://doi.org/10.1007/s11099-016-0206-x

Hassan I.A., 2006, Effects of water stress and high temperature on gas exchange and chlorophyll fluorescence in Triticum aestivum L, Photosynthetica, 44: 312-315

https://doi.org/10.1007/s11099-006-0024-7

Hauptherting S., and Fock H.P., 2000, Exchange of oxygen and its role in energy dissipation during drought stress in tomato plants, Physiologia Plantarum, 110: 489-495

https://doi.org/10.1111/j.1399-3054.2000.1100410.x

Hichri I., Muhovski Y., Zizkova E., Dobrev P., Francozorrilla J.M., Solano R., Lopezvidriero I., Motyka V., and Lutts S., 2014, The SlZF2 Cys2/His2 repressor-like zinc-finger transcription factor regulates development and tolerance to salinity in tomato and Arabidopsis

Khalekuzzaman M., Kim K.J., Kim H.J., Jung H.H., and Jang H.S., 2015, Comparison of green and variegated foliage plant species based on chlorophyll fluorescence parameters under different light intensities,

Krause G.H., and Weis E., 1984, Chlorophyll fluorescence as a tool in plant physiology, Photosynthesis Research, 5: 139

Li Q.M., Liu B.B., Wu Y., and Zou Z.R., 2008, Interactive effects of drought stresses and elevated CO2 concentration on photochemistry efficiency of cucumber seedlings, Bulletin of Botany, 50: 1307-1317

Liu H.X., Yan-You W.U., Sun W.H., Xing D.K., Zhao K., and Jing-Jie L.I., 2016, Effects of drought on photosynthesis and the physiological indices in tomato, Guihaia,

Maxwell K., and Johnson G.N., 2000, Chlorophyll fluorescence - a practical guide, Journal of Experimental Botany, 51: 659-668

Mccormick S., Niedermeyer J., Fry J., Barnason A., Horsch R., and Fraley R., 1986, Leaf disc transformation of cultivated tomato (L. esculentum) using Agrobacterium tumefaciens, Plant Cell Reports, 5: 81-84

https://doi.org/10.1007/BF00269239

Nr B., and E R., 2004, Applications of chlorophyll fluorescence can improve crop production strategies: an examination of future possibilities, Journal of Experimental Botany, 55: 1607

https://doi.org/10.1093/jxb/erh196

Rai A.C., Singh M., and Shah K., 2013, Engineering drought tolerant tomato plants over-expressing BcZAT12 gene encoding a C 2 H 2 zinc finger transcription factor, Phytochemistry, 85: 44

https://doi.org/10.1016/j.phytochem.2012.09.007

Shi H., Wang X., Ye T., Chen F., Deng J., Yang P., Zhang Y., and Chan Z., 2014, The Cysteine2/Histidine2-Type Transcription Factor ZINC FINGER OF ARABIDOPSIS THALIANA6 Modulates Biotic and Abiotic Stress Responses by Activating Salicylic Acid-Related Genes and C-REPEAT-BINDING FACTOR Genes in Arabidopsis, Plant Physiology, 165: 1367

https://doi.org/10.1104/pp.114.242404

Soto A., Hernández L., and Quiles M.J., 2014, High root temperature affects the tolerance to high light intensity in Spathiphyllum plants, Plant Science, 227: 84

https://doi.org/10.1016/j.plantsci.2014.07.004

Taiz L., and Zeiger E., 2010, Plant physiology, Quarterly Review of Biology, 167: 161-168

Xb J., and Tc H., 1988, Reduction of nitrite to nitric oxide by enteric bacteria, Biochemical and Biophysical Research Communications, 157: 106-108

https://doi.org/10.1016/S0006-291X(88)80018-4

Xu H., Gao J., Wang R., Li T.L., Ma J., and Liu M.C., 2011, Response of Water Stress on Chlorophyll Fluorescence Parameters of Tomato Seedlings, Chinese Agricultural Science Bulletin, 27: 189-193

Yordanov I., Velikova V., and Tsonev T., 1999, Influence of Drought, High Temperature, and Carbamide Cytokinin 4-PU-30 on Photosynthetic Activity of Bean Plants 1. Changes in Chlorophyll Fluorescence Quenching, Photosynthetica, 37: 447-457

https://doi.org/10.1023/A:1007163928253

Zhu J.K., 2002, Salt and drought stress signal transduction in plants, Annual review of plant biology, 53: 247

https://doi.org/10.1146/annurev.arplant.53.091401.143329