Under suitable cultivation conditions, the productivity of different crops is strongly related to the amount of light radiation intercepted in the crop canopy (Slattery and Ort, 2021), where excessive or insufficient amounts of light energy will have adverse effects on photosynthesis by crops (Ferrante and Mariani, 2018). Maize (Zea mays L.) is a light-loving and light-sensitive crop (Wang et al., 2016; Xue et al., 2019), but due to frequent extreme weather events in recent years, maize plants have experienced continuous low-temperature and rainy weather in the booting stage. These conditions can severely affect ear development and grain formation in maize, thereby resulting in large areas which high proportions of hollow straw and severe bald tip in some varieties (Huang et al., 2022), which are extremely unfavorable for agricultural production. Light is necessary for photosynthesis and it is the basis of plant life. Insufficient light will lead to decreases in the net photosynthetic rate (Pn) and partial chlorophyll fluorescence parameters in leaves (Qu et al., 2017; Wegrzyn and Mazur, 2020; Feng et al., 2021; Zahra et al., 2022). During this process, plant leaf cells undergo complex changes in physiological processes and cell metabolism, such as chloroplast decomposition, loss of photosynthetic activity, decomposition of chlorophyll and macromolecular compounds, and programmed cell death (Asad et al., 2019). These changes are associated with increases in intracellular reactive oxygen species (ROS) (Ramel et al., 2009). Insufficient light will accelerate leaf senescence and result in the excessive accumulation of ROS, oxidative damage to proteins, nucleic acids, and membrane lipids (Jbir-Koubaa et al., 2015), and decreases or losses of the activities of various enzymes (Mittler, 2002; Gill and Tuteja, 2010). As a consequence, the integrity of the cell membrane can be disrupted (Benlloch-Gonzalez et al., 2015), and the normal functions of chloroplast and mesophyll cells are eventually damaged, with decreased photosynthetic electron transport efficiency (Feng et al., 2021). Plants have a complete protective system of antioxidant enzymes that remove excessive ROS to protect the photosynthetic system and enhance adaptation to stress (Li et al., 2020).These enzymes include superoxide dismutase (SOD), and peroxidase (POD) (Dvorak et al., 2021). Thus, the antioxidant enzyme activity is an important indicator for evaluating whether the redox balance of plant cells is disrupted under adverse conditions (Gill et al., 2013).

The changes in the dependence of plant growth and development on light are regulated by plant hormones (Zhong et al., 2012). The changes in levels of plant hormones under shading are active responses by plants to adverse environments, and they provide the physiological basis that allows plants to make better use of assimilation products (Jiang et al., 2021). Gibberellin (GA) is necessary for the shade avoidance response in plants (Djakovic-Petrovic et al., 2007). In a previous study, we measured the changes in the contents of various hormones in two different light-sensitive inbred lines under shade treatment and in a control group without shade. According to the activities of the hormones, we found that the change in the gibberellin A₃ (GA₃) content was the most important. GA₃ is a type of tetracyclic diterpene plant hormone that can regulate many plant growth and development processes (e.g., seed germination, stem elongation, pollen maturation and fruit development), and one of its important functions is regulating the flowering time (Vicente and Plasencia, 2011). Previous studies of Arabidopsis showed that endogenous GA was necessary for flowering under non-induced conditions, and the flowering time was generally delayed in a GA synthesis defect mutant and GA signal transduction mutant (Rood et al., 1989; Ni and Bradford, 1993; Magome et al., 2004). Exogenous GA application can also promote flowering in Arabidopsis thaliana (Ezura and Harberd, 1995; Sauret-Gueto et al., 2012; Bao et al., 2020). It should also be noted GA is an excellent antioxidant that can enhance the tolerance of various biological and abiotic stresses by plants (Yamaguchi et al., 2014; Khan et al., 2015). GA₃ can also increase the number of cell divisions by activating the intermediate meristems to promote cell division (Mcatee et al., 2013). Guo et al. (2022) showed that spraying GA₃ could improve photosynthesis and the antioxidant defenses to increase the yield in salted wood pea. The exogenous application of GA₃ can delay the degradation of chlorophyll and protein, reduce the malondialdehyde (MDA) content, and delay plant senescence (Yu et al., 2009; Wang et al., 2015). Under low light stress, the abscisic acid (ABA) and zeatin (ZT) contents of soybean leaves decreased, whereas the indole acetic acid (IAA) and gibberellin (GA₃) contents increased. Similar results were obtained in previous studies of maize leaves under low light conditions, thereby suggesting that the response of this hormone to low light is an active stress response that allows plants to adapt to low light environments. Therefore, it is of great theoretical and practical significance to study the regulatory effects of exogenous GA₃ on different light-sensitive inbred maize lines under low light condition.

During the breeding of inbred maize lines over numerous years, we found and bred two inbred maize lines called SN98A and SN98B with extreme differences in their culms. In particular, the distinction, SN98A is called the “ear differentiation and sensitive to low light intensity inbred line”(ESL) and SN98B is called the “ear differentiation and insensitive to low light intensity near isogenic line” (EISL-NIL). Under low light stress condition, the hollowing rate in SN98A was 98% and that in SN98B was 0. Thus, in the present study, we used these weak light sensitive near-isogenic lines as experimental materials. By applying GA₃ to leaves, the regulation effect of exogenous GA₃ on empty stalk of maize under low light condition was analyzed. Through the analysis of photosynthetic response, antioxidant enzyme activity and other indexes, the purpose was to find out which physiological indexes of maize were affected by low light stress to induce maize stalk emptying. The regulatory effect of exogenous GA₃ on maize hollows under low light conditions and its regulatory mechanism were discussed, so as to provide solutions for poor maize yield under bad weather conditions.

Northeast China is the most important maize-producing area in China, where the maize output in this region account for more than 30% of the national maize output. In this region, light, heat, and water resources are generally abundant in the growing period. However due to global climate change, extreme weather events have become more frequent during the maize growing season, The frequency of overcast weather with high rain and low radiation during the withering and silking stage has recently increased each year (Yang et al., 2020), thereby adversely affecting the stability of the maize yield in Northeast China. Light is essential for photosynthesis by plants and the basis for plant growth and development (Jiang et al., 2021). Maize is a light-loving crop with no obvious light saturation point and it is very sensitive to changes in the light intensity. A lack of light during tasseling will inhibit the normal physiological activities, decrease photosynthesis in the leaves, and cause cell metabolism disorders and REDOX homeostasis damage, thereby leading to problems such as ear bald tip, yield reductions, and even hollow stalks. Low light stress can accelerate the excessive accumulation of ROS in maize leaves and cause the peroxidation of membrane lipids. Colebrook et al. (2014) indicated that hormones can effectively help plants to cope with abiotic stress, where stress responses are regulated mainly by activating specific hormones via signal transduction and crosstalk in different developmental environments (Verma et al., 2016). Therefore, how to increase the yield and reduce the empty stalk rate under the condition of insufficient light has become an important problem.

GA₃ is a plant growth regulator and it is involved in the response to many abiotic stresses in plants, with positive regulatory effects on plant growth and development (Bao et al., 2020). Exogenous GA₃ application can reduce the effects of nickel stress (Wiszniewska et al., 2018) and increase the plant cell length independent of biosynthesis (Rizza et al., 2017). In addition, GA and photoperiod pathways have been shown to synergistically regulate crop flowering under long sunshine conditions (Fukuda et al., 2012; Wang et al., 2016). In the present study, GA₃ treatment reduced the hollow stem rate in maize by regulating the flowering interval between male and female ears, where treatment with 60 mg L^–1 GA₃ had the greatest effect, followed by treatment with 40 mg L^–1 GA₃ and 20 mg L^–1GA₃. Under shading treatment, the H₂O₂ and O 2 – contents continued to increase in the SN98A control group, and the contents were always higher than those in SN98B. After GA₃ spraying treatment, the O 2 – production rate and H₂O₂ contents still increased in SN98A and SN98B, but the increases were significantly smaller than those in the control group, and the O 2 – production rate and H₂O₂ contents were always lower in SN98B than SN98A due to the photoprotective capacity of the shade-tolerant inbred line SN98B. Low light stress can induce oxidative stress in maize, but GA₃ treatment can enhance the ability of maize to resist low light stress and reduce the oxidative pressure caused by insufficient light. Numerous studies have shown that membrane lipid peroxidation leads to the accumulation of MDA. Low light stress can disrupt the dynamic equilibrium between ROS production and scavenging in plants, thereby resulting in the accumulation of ROS and increased membrane permeability. As a consequence, membrane lipid peroxidation lead to the accumulation of MDA and exacerbates maize aging (Wang et al., 2021). In this study, GA₃ treatment significantly reduced the MDA contents of the two inbred lines under low light. The MDA contents were higher in SN98A than SN98B in both the control and treatment groups. The antioxidant enzyme system in plants protects against the toxic effects of ROS. SOD and POD are important antioxidant enzymes in the plant defense mechanism. GA₃ may have reduced the ROS contents in maize by enhancing the activities of POD and SOD in the light-sensitive inbred line SN98A, as also suggested by Ali et al. (2021). APX, Fe-SOD and GR are important genes related to the activities of antioxidant enzymes (Lee et al., 2007). Studies have shown that the overexpression of APX, Fe-SOD, and GR significantly improved the tolerance of abiotic stresses by transgenic tall fescue plants. In the present study, we found that exogenous GA₃ treatment significantly upregulated the expression levels of APX and GR in SN98A and SN98B compared with the control group, thereby indicating that exogenous GA₃ could enhance the activities of antioxidant enzymes to resist external abiotic stress by increasing the expression of antioxidant-related genes. Therefore, exogenous GA₃ may improve the tolerance of stress in plants by regulating antioxidant metabolism and reducing the lipid peroxidation of cell membranes (Gilroy and Jones, 1992; Jiang and Huang, 2001) to decrease the damage due to low light stress in plants. According to the expression level of GA-related genes, the gene pathway of gibberellin signaling is GA-GID1-DELLA signaling pathway. When gibberellin is at a high level, GID1 can sense the GA signal and combine with it to form GA-GID1. Then it binds to DELLA protein to form GID1-GA-DELLA complex trimer (Zentella et al., 2007), so that ubiquitin ligase SCF in F-Box protein can bind to DELLA protein GRAS region (Fleet and Sun, 2005). The rapid degradation of DELLA protein through ubiquitin proteomic channels resulted in the release of its repression and normal gibberellin response in plants. Therefore, the reduction of gibberellin receptor GID1 may also affect the degradation of DELLA protein at the protein level. After exogenous GA₃ was applied, the expression of GA20ox2, a gene related to gibberellin synthesis, decreased (FIG 9G). GA20ox2 plays an important role in the synthesis of gibberellin in higher plants, and the decreased expression of GA20ox gene may decrease the production of endogenous gibberellin. In CK group, the expression level of gibberellin-synthesis-related genes in SN98A was lower than that in SN98B, and CKA of degradation-related genes was higher than that in CKB. Therefore, low light stress inhibited the synthesis of gibberellin by decreasing the expression of genes related to gibberellin synthesis and enhancing the expression of genes related to degradation, resulting in empty culms.

The responses of photosynthetic organs to low light stress and the associated mechanisms are important for understanding the adaptation of crops to different light environments. Thus, many studies have investigated the self-regulation mechanism and light energy conversion process in maize under low light conditions (Zivcak et al., 2014; Hazrati et al., 2016; Yamori, 2016). Chloroplasts are the site of photosynthesis in plants. Weak light stress can significantly damage the anatomical structure of plants to directly affect normal photosynthetic electron transport and the photosynthetic rate (P_n) (Du et al., 2011; Feng et al., 2021). Under low light, the oxidative pressure is intensified in maize leaves and the accumulation of large amounts of ROS leads to changes in the spatial configurations of various enzymes in chloroplasts, thereby adversely affecting their function, decreasing the chlorophyll content, and inhibiting photosynthesis. In the present study, under shading treatment, the Chl a, Chl b and chlorophyll (a+b) contents, tended to increase initially and then decrease in SN98A, whereas the Chl contents did not change greatly in SN98B and they were always higher than those in SN98A. After GA₃ treatment, the photosynthetic pigment contents increased significantly in SN98, and the Pn, Tr, and Gs values were also significantly higher compared with those in the control. PSII is one of the primary sites in photosynthetic organs damaged by stress, and it plays important roles in the light energy conversion and electron transport processes. (Zhang et al., 2020). The photoreaction requires coordination of the photosynthetic system in order to complete the normal linear electron transfer and provide the homogeneity for the fixation and reduction of CO₂ in the dark reaction. (Qian et al., 2017). In the present study, Pn, qP, and Φ_PSII continued to decrease during shading in SN98A, whereas they tended to increase initially and then decrease in SN98B, but the values were always higher than those in SN98A, thereby indicating that the normal photosynthetic physiological process was maintained in SN98B. GA₃ treatment could have increased the stomatal conductivity of the maize leaves, enhanced the photosynthetic activity of mesophyll cells, and improved the photosynthetic capacity of maize leaves (Verma et al., 2016), where 60 mg L^–1 GA₃ treatment had the greatest effect, and thus GA₃ may be involved in the shade protection response process in maize leaves. GA₃ had a positive effect on the photosynthetic efficiency of maize leaves under low light stress.

Plant photosynthesis is an extremely complex physiological process and it is negatively affected by both biological and abiotic stresses. The main limiting factors for photosynthesis are light and carbon dioxide (Smith, 1938). Under low light stress, photosynthesis is inhibited in crops and yields are reduced (Liu et al., 2020). In the present study, under low light stress, Pn, Tr, and Gs all decreased with time during shading, in the SN98A control group and the intercellular carbon dioxide concentration increased. Applying GA₃ improved Pn, Tr, and Gs in SN98A and reduced the intercellular carbon dioxide concentration, where the effect of 60 mg L^–1 GA₃ was most significant. Low light stress also reduced Pn, Tr, and Gs in the leaves in the SN98B control group, and increased the intercellular carbon dioxide concentration, but the normal physiological activities were generally maintained.

In the present study, maize inbred lines SN98A and SN98B with differences in their light sensitivity were subjected to shading in the maize tasseling stage ( Figure 10 ). We found that low light treatment reduced the photosynthetic capacity of the maize leaves and inhibited the transport of photosynthetic products to other organs, thereby resulting in plant growth inhibition and leaf senescence. The adverse effects of shading were significantly greater in the weak light-sensitive inbred line SN98A than SN98B, mainly because SN98A had a significantly higher hollow stem rate than SN98B after shading. GA is an excellent antioxidant that can improve the tolerance of various biological and abiotic stresses in plants. These findings help us to understand the physiological mechanisms in maize inbred lines with differences in photosensitivity that mediate the response to low light stress under treatment with exogenous GA. The photosynthetic performance parameters of plants, i.e., Pn, Tr, Gs, photosynthetic pigment contents, (Fv/Fm), qP, and Φ_PSII, improved after applying GA₃ (20 mg L^–1, 40 mg L^–1, and 60 mg L^–1) to the leaves, including 60 mg L^-1 GA₃ works best. Thus, the foliar application of GA₃ to SN98A and SN98B will be beneficial for their growth and development under lower light conditions.

The original contributions presented in the study are included in the article/ Supplementary Material . Further inquiries can be directed to the corresponding author.

JF: investigation, data curation, validation, and writing—original draft; LL: review and editing; SW: data curation, methodology, formal analysis, and software; NY: formal analysis and editing; HS: investigation and formal analysis; ZS: resources and funding acquisition; FL: writing—review and editing; XZ: conceptualization, writing—review, editing and funding acquisition. All authors contributed to the article and approved the submitted version.