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Yield, cell structure and physiological and biochemical characteristics of rapeseed under waterlogging stress

BMC Plant Biology volume 24, Article number: 941 (2024) Cite this article

Abstract

Rapeseed (Brassica napus L.) is a major oilseed crop in the middle and lower reaches of the Yangtze River in China. However, it is susceptible to waterlogging stress. This study aimed to investigate the physiological characteristics, cellular changes, and gene expression patterns of rapeseed under waterlogging stress, with the goal of providing a foundation for breeding waterlogging-tolerant rapeseed. The results revealed that waterlogging-tolerant rapeseed exhibited higher levels of soluble sugars and antioxidant enzyme activity, particularly in the roots. Conversely, waterlogging-sensitive rapeseed displayed greater changes in malondialdehyde, proline, and hydrogen peroxide levels. Cellular observations showed that after experiencing waterlogging stress, the intercellular space of rapeseed leaf cells expanded, leading to disintegration of mitochondria and chloroplasts. Moreover, the area of the root xylem increased, the number of vessels grew, and there were signs of mitochondrial disintegration and vacuole shrinkage, with more pronounced changes observed in waterlogging-sensitive rapeseed. Furthermore, significant differences were found in the transcription levels of genes related to anaerobic respiration and flavonoid biosynthesis, and different varieties demonstrated varied responses to waterlogging stress. In conclusion, there are differences in the response of different varieties to waterlogging stress at the levels of morphology, physiological characteristics, cell structure, and gene transcription. Waterlogging-tolerant rapeseed responds to waterlogging stress by regulating its antioxidant defense system. This study provides valuable insights for the development of waterlogging-tolerant rapeseed varieties.

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Introduction

China is one of the largest countries in terms of rapeseed (Brassica napus L.) cultivation area, maintaining approximately 100 million mu (1 hectare = 15 mu) annually [1, 2]. The Yangtze River Basin, a predominant cultivation region, which accounts for over 70% of the production and cultivation area [3]. Particularly in the middle and lower reaches of the Yangtze River, the “rice-oil” rotation system is prevalent, with some areas even adopting a “rice-rice-oil” triple cropping system, resulting in high groundwater levels in these regions [4]. Combined with frequent rainfall and a damp, cold climate during the rapeseed cultivation period, substantial waterlogging stress often occurs [5]. Waterlogging stress restricts gas exchange in the soil, leading to concurrent hypoxia stress. Rapeseed is sensitive to waterlogging and hypoxia stress due to the absence of aeration tissues. This stress adversely affects rapeseed growth and yield, with potential yield losses exceeding 40% in severe cases [6]. Currently, common practices to alleviate waterlogging stress in production include intertillage and deep ditching, but these methods are labor-intensive and show limited effectiveness [4]. Therefore, studying cost-effective strategies for waterlogging tolerance, improving the ability of rapeseed to withstand waterlogging stress, and breeding waterlogging-tolerant rapeseed varieties remain of significant importance.

Waterlogging, also known as wet damage, refers to the condition in which soil moisture content is excessively high or reaches saturation, resulting in a low-oxygen or anoxic environment that hampers plant growth [7]. This condition leads to the accumulation of anaerobic respiration byproducts and reactive oxygen species in plants, causing toxicity and oxidative damage [8]. Initially, it affects the root system, leading to decreased root vitality, obstruction of energy supply and nutrient transport, and disruption of membrane integrity [9, 10]. Waterlogging stress also inhibits the growth of soybean nodules, with its impact being less significant on tolerant varieties compared to intolerant ones. Furthermore, waterlogging induces physiological and morphological changes in leaves. Prolonged waterlogging significantly increases soybean leaf conductivity, malondialdehyde, and proline levels [11]. In cotton, waterlogging stress weakens photosynthesis, reduces chlorophyll synthesis, and lowers chlorophyll content [12]. Leaves of plants such as cotton [12], poplar [13], watermelon [14], alfalfa [15], and sesame [16], exhibit yellowing and wilting phenotypes after waterlogging stress. Additionally, the number of leaves and biomass of cucumber [17], tomato [18], and wheat [19], significantly decrease after experiencing waterlogging stress. Moreover, waterlogging stress affects plant cells, leading to chloroplast membrane rupture, thylakoid membrane vacuolization, and tonoplast invagination or rupture [12, 20]. Rice subjected to waterlogging stress suffers from cell membrane damage, increased membrane permeability, leakage of cellular contents, and metabolic disorders [21].

Therefore, it is indispensable to discover efficacious approaches to enhance plant tolerance against waterlogging stress. Flavonoids are capable of effectively eliminating reactive oxygen species and free radicals within plants, and alleviating the damage induced by oxidative stress [22, 23]. Some investigations have shown that exogenous flavonoids can efficaciously improve the antioxidant capacity of plants. For instance, the treatment of litchi fruits with exogenous proanthocyanidin can enhance their antioxidant capacity and postpone peel browning [24]. The application of exogenous epigallocatechin gallate (EGCG) can augment the active oxygen scavenging ability of tea and boost the tolerance of tea plants to cold stress [25]. Nevertheless, the application of exogenous flavonoids can decrease peroxidase activity and malondialdehyde content in wheat, thereby mitigating the harm of powdery mildew to plants [26]. Possibly, exogenous flavonoids might also exert a positive effect on rapeseed waterlogging resistance, yet there are scarce studies in this regard.

In recent years, research on plant tolerance to waterlogging stress has gained significant attention. However, studies on the mechanism of waterlogging tolerance in rapeseed have primarily focused on screening tolerant materials, quality effects, physiological and biochemical changes, and transcriptomics. There has been little systematic exploration of the physiological and biochemical changes, cell changes, and gene expression alterations in rapeseed under waterlogging stress.

In this study, both waterlogging-sensitive and waterlogging-tolerant rapeseed varieties were used as experimental materials. Comprehensive analyses were conducted on root and leaf phenotypes, physiological and biochemical changes, cell alterations, relative transcription levels of oxidative stress-related genes, and the effects of exogenous antioxidants on rapeseed under waterlogging stress during the seedling stage. This multi-level approach aimed to elucidate the mechanisms by which different varieties of rapeseed respond to waterlogging stress, thereby providing theoretical guidance for enhancing rapeseed tolerance to waterlogging stress and for breeding waterlogging-tolerant rapeseed varieties.

Results

The effects of waterlogging stress on the growth of rapeseed

Phenotypic analysis of rapeseed seedlings after waterlogging stress revealed that waterlogging severely affected the growth of the waterlogging-sensitive variety G218. Compared to the control check (Fig. 1B), the flooded rapeseed plants exhibited stunted growth, reduced biomass, yellowing and purpling of oldest leaves, and abnormal root development (Fig. 1A). In contrast, the waterlogging-tolerant variety G230 showed better growth and was less affected by waterlogging stress, with only a small number of older leaves losing their green color (Fig. 1A).

Fig. 1
figure 1

Seedling morphology of two varieties of rapeseed after 6d of waterlogging stress. (A) G218 and G230 seedlings after waterlogging stress; (B) G218 and G230 seedlings under normal irrigation conditions. WS: The waterlogging stress treatment; CK: The control check

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Six days after the stress period, the flooded rapeseed plants recovered normal growth. Analysis of the harvested seeds revealed significant decreases in oil acid and protein content in G218 seeds (Fig. 2A), while G230 seeds showed no apparent influence (Fig. 2B). Additionally, mature rapeseed plants were analyzed for the number of pods per plant (Fig. 2C), plant height (Fig. 2D), thousand-grain weight (Fig. 2E), and individual seed weight (Fig. 2F). The results showed significant decreases in thousand-grain weight, plant height, pods per plant, and individual seed weight in G218, while no significant changes were observed in G230. These findings indicate that waterlogging stress severely affects the growth and quality of the waterlogging-sensitive rapeseed variety.

Fig. 2
figure 2

Effects of waterlogging stress on the growth and productivity of different varieties of rapeseed. (A) Analysis of seed components of G218; (B) Analysis of seed components of G230; (C) Analysis of the number of pods of G218 and G230; (D) Analysis of the plant height of G218 and G230; (E) Analysis of the thousand grain weight of G218 and G230; (F) Analysis of the seed weight per plant of G218 and G230. WS: The waterlogging stress treatment; CK: The control check. Different lowercase letters indicate significant differences at the 0.05 probability level

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Observation of rapeseed tissue structure under waterlogging stress

To investigate the effects of waterlogging stress on the tissue structure of rapeseed, the cell structures of roots and leaves were stained with safranin-O fast green. Observation of leaf cell structure revealed that, compared to the normally grown G218 (Fig. 3B) and G230 (Fig. 3D) leaves, the G218 leaves exhibited spongy tissue and palisade tissue with enlarged intercellular spaces after waterlogging stress (Fig. 3A). In contrast, there were no significant changes in the leaf structure of G230 (Fig. 3C). Observation of root structure showed that, compared to the normally grown G218 (Fig. 4B) and G230 (Fig. 4D) root structures, the G218 (Fig. 4A) and G230 (Fig. 4C) roots had significantly increased xylem area and an increased number of vessels, though the diameter of individual vessels was smaller after waterlogging stress, especially in G230. Notably, regardless of waterlogging stress or normal growth conditions, the spongy tissue and palisade tissue in G230 leaves were arranged more tightly than in G218. In the roots, G230 had more vessels and smaller individual vessel diameters compared to G218 (Table 1). These results indicate that waterlogging stress affects the cellular structure of rapeseed tissues and that variations in waterlogging sensitivity led to differences in the structural responses of different rapeseed varieties.

Fig. 3
figure 3

Observing the anatomical structure of G218 and G230 leaves using safranin o-fast green staining. (A) G218 waterlogging stress treatment; (B) G218 control check; (C) G230 waterlogging stress treatment; (D) G230 control check

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Fig. 4
figure 4

Observing the anatomical structure of G218 and G230 roots using safranin o-fast green staining. (A) G218 waterlogging stress treatment; (B) G218 control check; (C) G230 waterlogging stress treatment; (D) G230 control check. P: Phloem. Xy: Xylem. Sx: Secondary xylem. VE: Vessel

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Table 1 Comparison of tissue structure of two varieties of Brassica napus L. G218 and G230 under waterlogging stress
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Observation of rapeseed cell ultrastructure under waterlogging stress

To further investigate the effects of waterlogging stress on rapeseed cells, transmission electron microscopy was employed to examine root and leaf cells.

Observation of leaf cell ultrastructure revealed that under control treatment, in leaf cells of G218 (Fig. 5A, B, C) and G230 (Fig. 6A, B, C), all organelles were clearly visible. Chloroplasts exhibited spindle-shaped forms near the cell membrane, containing few starch grains and osmiophilic granules, with well-organized thylakoid structures and distinct lamellar arrangements. Mitochondria appeared spherical, predominantly distributed near the chloroplasts. Under waterlogging stress treatment, in G218 leaf cells, organelles remained visible but exhibited deformities in some chloroplasts, disarrayed thylakoid lamellae, increased starch grains and osmiophilic granules, and partial mitochondrial degradation (Fig. 5D, E, F). In contrast, G230 leaf cells showed clear organelle structures and normal cell morphology with minimal deviation from control treatment (Fig. 6D, E, F). Ultrastructure observations of root cells indicated that under control treatment, the root cells of G218 (Fig. 7C, D) and G230 (Fig. 8C, D) were closely arrayed, with each cell organelle being clearly distinguishable, large vacuoles in the middle, and many round mitochondria distributed near the cell membrane. After waterlogging stress, the root cells of G218 and G230 remained closely arranged, each organelle was clearly visible, and mitochondria were short rod-shaped or spheroidal. However, compared with the control treatment, vacuole shrinkage and mitochondrial disintegration occurred in G218 cells (Fig. 7A, B). Similarly, a small number of mitochondria began to disassemble in G230 cells, and larger peroxisomes were produced (Fig. 8A, B).

These findings indicate that waterlogging stress causes significant damage to rapeseed cells, potentially affecting their photosynthesis and respiration, especially in waterlogging-sensitive varieties.

Fig. 5
figure 5

Transmission electron microscopy observation of G218 seedling leaves. (A) (B) (C) Control treatment; (D) (E) (F) waterlogging stress treatment. N: Nucleus; CW: Cell wall; Ch: Chloroplast; Mi: Mitochondria; S: Starch granules; GL: Grana lamella; OG: Osmiophilic granules

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Fig. 6
figure 6

Transmission electron microscopy observation of G230 seedling leaves. (A) (B) (C) Control treatment; (D) (E) (F) waterlogging stress treatment. N: Nucleus; CW: Cell wall; Ch: Chloroplast; Mi: Mitochondria; S: Starch granules; GL: Grana lamella; OG: Osmiophilic granules

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Fig. 7
figure 7

Transmission electron microscopy observation of G218 seedling root system. (A) (B) Waterlogging stress treatment; (C) (D) Control treatment. N: Nucleus; CW: Cell wall; Mi: Mitochondria; V: Vacuole

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Fig. 8
figure 8

Transmission electron microscopy observation of G230 seedling root system. (A) (B) Waterlogging stress treatment; (C) (D) Control treatment. N: Nucleus; CW: Cell wall; Mi: Mitochondria; V: Vacuole; PE: Peroxisome

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Analysis of transcription levels of waterlogging-related genes in different tissues of rapeseed

Rapeseed plants often undergo hypoxic or anoxic stress when exposed to waterlogging conditions. In this study, we examined the transcription levels of genes related to anaerobic respiration in response to this stress. Our results revealed that under normal growth conditions (CK), there were no significant differences in the transcription levels of anaerobic respiration-related genes ALDH3F1 and AAE2 between the root and leaf tissues of two distinct stress-tolerant rapeseed varieties. However, the expression of the ADHL7 gene in the waterlogging-tolerant rapeseed variety G230 was significantly lower compared to the waterlogging-sensitive variety G218. Following the waterlogging stress, we observed a significant increase in the relative transcription levels of anaerobic respiration-related genes ALDH3F1, ADHL7, and AAE2 in the leaf and root of both G218 and G230. Notably, there was a more pronounced upregulation in the transcription levels of the ADHL7 gene in the root and leaf tissues of G230 compared to G218 (Fig. 9A, B, C).

Cell observations and physiological indicator analyses demonstrated that under waterlogging stress, the waterlogging-tolerant rapeseed variety G230 exhibited superior reactive oxygen species scavenging ability compared to the waterlogging-sensitive variety G218. Given the strong antioxidant properties of flavonoids, we examined the transcription levels of genes associated with flavonoid biosynthesis pathways. The results indicated that the relative transcription levels of the chalcone isomerase-related gene FAP3 and the vacuolar sorting receptor-related gene VSR7 were significantly upregulated in both root and leaf tissues following stress-induced damage. Notably, this upregulation was more pronounced in the leaf tissues than in the root tissues (Fig. 9D, E). Specifically, the relative transcription level of the VSR7 gene was markedly upregulated in both root and leaf tissues of G230, significantly surpassing its levels in G218. Additionally, the relative transcription level of the anthocyanin biosynthesis-related gene LDOX was significantly upregulated only in the leaf tissues of G218 following waterlogging-induced damage, with no significant changes observed in the root tissues of G218 or in any tissues of G230 (Fig. 9F).

These results indicate that waterlogging stress induces changes in the transcription levels of genes related to anaerobic respiration and flavonoid biosynthesis in rapeseed, leading to alterations in cell structure and intracellular substances. These changes vary between different varieties of rapeseed, resulting in differing sensitivities to waterlogging stress and significant phenotypic differences.

Fig. 9
figure 9

Relative transcription levels of glycolytic-related genes and flavonoid biosynthesis-related genes in two varieties of rapeseed under waterlogging stress. (A) (B) (C) Relative transcription levels of glycolytic-related genes. (D) (E) (F) Relative transcription levels of genes related to flavonoid biosynthesis. Different lowercase letters indicate significant differences at the 0.05 probability level

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Effects of exogenous antioxidants on rapeseed under waterlogging stress

To investigate methods for enhancing the waterlogging resistance of rapeseed, we applied exogenous antioxidants to the leaves and analyzed their effects on waterlogging resistance. Epicatechin (EC), a flavonoid with antioxidant properties, was selected for this study. We sprayed the leaves of G230 and G218 rapeseed varieties with distilled water (WT) and a 5µmol/L epicatechin (EC) solution, respectively, when the seedlings reached the five-leaf stage, followed by sustained waterlogging stress. The results indicated that most leaves of G230 began to show significant de-greening on the 10th day of waterlogging stress, becoming completely yellow and shedding by the 20th day (Fig. 10A). This was consistent with the phenotypic changes observed in G230 seedlings sprayed with distilled water (WT) (Fig. 10B). For G218, leaf chlorosis and yellowing began on the 6th day of stress, with leaf loss and biomass reduction occurring by the 10th day. The seedlings wilted and nearly died by the 20th day (Fig. 10A). In G218 seedlings treated with distilled water (WT), leaf greening, yellowing, and curling began on the 6th day of waterlogging, followed by leaf shedding on the 10th day, with the plants wilting and dying by the 14th day (Fig. 10B).

Fig. 10
figure 10

Effects of foliar spraying of flavonoids on simulated waterlogging stress in rapeseed. (A) External application of epicatechin (EC); (B) External application of water (WT)

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In addition, we assessed the levels of malondialdehyde (MDA) (Fig. 11A), proline (Pro) (Fig. 11B), soluble sugars (Fig. 11C), peroxidase (POD) (Fig. 11D), superoxide dismutase (SOD) (Fig. 11E), and hydrogen peroxide (H2O2) (Fig. 11F) in both the roots and leaves of G218 and G230 under normal growth conditions, waterlogging stress, and exogenous EC spraying treatments. Compared to the normal growth conditions (CK), waterlogging stress (WS) resulted in a significant increase in MDA content, soluble sugar content, H2O2 content, POD activity, and SOD activity, while Pro content significantly decreased in both the roots and leaves of both rapeseed varieties. However, some variations were observed between different varieties of rapeseed. The increase in MDA and H2O2 contents was more pronounced in G218, whereas the increase in POD and SOD activities was more prominent in G230. Furthermore, compared to the various indicators under waterlogging stress (WS), the application of exogenous EC (WS + EC) led to a significant decrease in MDA in the leaves of G218. Simultaneously, the Pro content significantly increased in the roots and leaves of both rapeseed varieties, while H2O2 content decreased. Additionally, soluble sugar content significantly increased in both the roots and leaves of G218. POD activity showed a significant increase in the leaves of both G218 and G230, while SOD activity increased significantly in the leaves of G218 and in both the roots and leaves of G230.

These findings suggest that waterlogging stress induces oxidative stress in rapeseed, leading to alterations in osmotic regulation and antioxidative systems. Waterlogging-tolerant rapeseed varieties demonstrate enhanced capacity to regulate antioxidative enzyme activity, thereby alleviating waterlogging stress. Moreover, exogenous EC application can enhance rapeseed tolerance to waterlogging stress by augmenting antioxidative enzyme activity and osmotic regulation capacity.

Fig. 11
figure 11

Biochemical changes of rapeseed after waterlogging stress. (A) Changes in MDA content; (B) Changes in Pro content; (C) Changes in soluble sugar content; (D) Changes in POD activity; (F) Changes in SOD activity; (F) Changes in H2O2 content. CK: The control check; WS: The waterlogging stress treatment. WS + EC: Exogenous epicatechin was sprayed after waterlogging stress. Different lowercase letters indicate significant differences at the 0.05 probability level

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Discussion

Effects of waterlogging on rapeseed phenotype and oil quality

Waterlogging has various effects on rapeseed, including aboveground growth, belowground development, and rapeseed yield and quality [10]. Waterlogging stress impacts different stages of rapeseed growth, particularly during the seedling and flowering stages. During the seedling stage, waterlogging stress significantly reduces root thickness, length, total root number, green leaf number, leaf area, and dry weight of rapeseed [4, 10, 27]. This study also found that waterlogging stress adversely affects rapeseed by reducing the number of green leaves and biomass of seedlings and causing abnormal root development. This effect is especially pronounced in waterlogging-sensitive rapeseed, severely restricting seedling growth.

Waterlogging stress during emergence and budding stages significantly reduces the number of siliques per plant, grains per silique, primary branches, and overall yield of rapeseed [28]. Another study also found that waterlogging stress during the budding stage severely damages the main inflorescence [29]. Moreover, waterlogging stress during the bud formation, flowering, and pod development stages affects the number of primary branches and effective siliques [30]. Previous studies suggest that short-term waterlogging stress during the flowering and fruiting stages affects rapeseed yield by influencing the number of effective siliques and thousand grain weight, while having minimal effect on oil content. However, long-term and persistent waterlogging stress negatively impacts oil content [31]. Other researchers have shown that waterlogging stress during the initial flowering stage of rapeseed not only affects yield but also degrades oil quality, increasing the erucic acid and glucosinolate content in the seeds [32].

In our study, we investigated the growth status and oil quality of rapeseed after waterlogging stress during the seedling stage. We found that waterlogging stress during the seedling stage had effects on rapeseed plant height, number of pods per plant, thousand grain weight, and individual seed weight. However, there were significant differences among rapeseed varieties with different tolerance to waterlogging. These parameters significantly decreased in waterlogging-sensitive rapeseed, while they were largely unaffected in waterlogging-tolerant rapeseed, which is consistent with previous studies. Furthermore, there were no significant changes in seed oil content, linoleic acid content, and protein content, but oleic acid content decreased, especially in waterlogging-sensitive rapeseed. The results indicate that waterlogging stress affects the growth of rapeseed roots and leaves, resulting in abnormal plant and seed development, and subsequently influencing oil quality.

Rapeseed cell structure is regulated by osmotic adjustment substances and antioxidant enzyme activity, thereby affecting rapeseed tolerance to waterlogging stress

When plants are subjected to waterlogging stress, the root system often encounters low oxygen or anaerobic environments, causing the roots to switch from aerobic respiration to anaerobic respiration [33, 34]. Anaerobic respiration can lead to the accumulation of substances such as ethanol and lactic acid, causing cytoplasmic acidosis and harming plant growth [35]. Waterlogging stress and anaerobic respiration can cause root damage, resulting in decreased antioxidant enzyme activity, oxidative bursts, increased cell membrane permeability, and mitochondrial disintegration, leading to cellular damage [33, 36,37,38]. Studies have also shown that waterlogging stress affects the root cell cytoskeleton of rapeseed, damages root cell ultrastructure, and alters the reactive oxygen species scavenging system [10]. Additionally, waterlogging stress and anaerobic respiration can impact photosynthesis in leaves. Plants subjected to waterlogging stress will close stomata, leading to metabolic disorders and a decrease in photosynthetic rate [39].

To investigate the specific mechanisms of rapeseed damage under waterlogging stress, we analyzed the activity of antioxidant enzymes, changes in reactive oxygen species, osmotic adjustment substance content, and cell structure in different tissues of rapeseed. The results showed that waterlogging stress significantly increased the content of antioxidant enzymes, membrane lipid peroxidation products, and reactive oxygen species in the roots and leaves of rapeseed, with differences observed among varieties with varying waterlogging tolerance. Tolerant rapeseed exhibited better reactive oxygen species homeostasis and higher antioxidant enzyme activity. Additionally, the content of osmotic adjustment substances, such as proline (Pro) and soluble sugars, also changed in the roots and leaves. Observations of root cell changes in rapeseed varieties with different waterlogging tolerance after waterlogging stress revealed that the area of the xylem tissue in the roots increased, the number of vessels increased, but the cross-sectional area of the vessels became smaller. These changes were more pronounced in tolerant rapeseed varieties.

Xylem tissue and vessels transport water and nutrients from the underground to the aboveground parts of rapeseed [40], and the changes in the root system after waterlogging stress may be an adaptation of rapeseed to cope with this stress. Ultrastructural observations of root cells showed mitochondrial disintegration and vacuole shrinkage, indicating that waterlogging stress affects the aerobic respiration and osmotic regulation capacity of rapeseed roots. Observation of leaf cells in rapeseed with different waterlogging tolerance after waterlogging stress revealed that the palisade tissue and spongy tissue in the leaves became noticeably looser, particularly in sensitive varieties. Leaves are the primary sites of photosynthesis, and research has shown that the photosynthetic rate is related to the arrangement of palisade and spongy tissues in leaves, with leaf thickness being positively correlated with the photosynthetic rate [41]. This suggests that waterlogging stress may severely affect the photosynthesis of rapeseed, especially in sensitive varieties. Ultrastructural changes in leaf cells also showed partial mitochondrial disintegration, disordered thylakoid membrane structure, and increased accumulation of osmiophilic particles, which were more pronounced in sensitive varieties of rapeseed. Osmiophilic particles result from the aggregation of degradation products of plastid lipids and serve as indicators of the degree of leaf cell damage [42, 43]. This indicates that waterlogging stress severely damages the leaf cells of sensitive rapeseed varieties. The changes in mitochondria and chloroplasts also indicate a significant impact on photosynthesis and respiration in leaves. In conclusion, our results suggest that waterlogging stress affects the osmotic regulation capacity and reactive oxygen species scavenging ability of rapeseed roots, thereby impacting minerals transport, photosynthesis, and respiration. Rapeseed variety G230, however, maintains stable material transport and normal photosynthetic and respiratory functions under waterlogging stress through adjustments in its root xylem and vascular tissues. This adaptation helps maintain cellular oxidative balance and enhances tolerance to waterlogging stress.

Exogenous antioxidants can effectively enhance the waterlogging tolerance of rapeseed plants

Under stress conditions, plants produce various antioxidants that regulate reactive oxygen species levels and protect cells from damage, thereby alleviating and adapting to various stresses. Enhancing plant antioxidant capacity is a common method to improve plant stress tolerance, and many exogenous growth regulators play an important role in this process. Research has shown that the triazole substance S3307 can effectively improve the antioxidant capacity of waterweed (Malachium aquaticum) and soybean, enhancing their resistance to stress [44, 45]. Exogenous melatonin can regulate the antioxidant defense of rapeseed and enhance its tolerance to cobalt toxicity [46]. Additionally, exogenous anthocyanins can enhance the antioxidant enzyme activity of tobacco, thereby improving its drought resistance [47].

This study found that the relative transcription levels of certain anaerobic respiration-related genes in rapeseed were significantly upregulated in both roots and leaves under waterlogging stress, indicating that the plants were subjected to hypoxia or anoxia stress. Additionally, some genes involved in flavonoid biosynthesis showed significant changes in their relative transcription levels, with different response patterns observed among waterlogging-tolerant rapeseed varieties. These findings suggest that flavonoids may play a key role in rapeseed waterlogging tolerance.

Currently, methods to improve plant waterlogging tolerance generally involve breeding waterlogging-tolerant rapeseed varieties and implementing measures such as tillage and drainage, with limited research on the role of exogenous growth regulators in enhancing waterlogging tolerance. Our previous study demonstrated that exogenous vitamin B6 can enhance rapeseed waterlogging tolerance by improving its reactive oxygen species scavenging ability [27]. To explore the role of flavonoids in rapeseed waterlogging tolerance further, this study found that exogenous flavonoids, such as epicatechin sprayed on leaves, have a similar effect to vitamin B6 by regulating the antioxidant defense system, thereby enhancing waterlogging tolerance.

In summary, waterlogging stress in rapeseed often accompanies hypoxia or anoxia stress, promoting anaerobic respiration, causing reactive oxygen species outbreaks, cell damage, and affecting root and leaf growth and development. However, rapeseed alleviates and adapts to waterlogging stress by enhancing its antioxidant defense systems, including reactive oxygen species scavenging systems, vitamin B6 metabolism, and flavonoid biosynthesis.

Materials and methods

Materials and stress treatment

Waterlogging-tolerant Brassica napus L. (G230) and waterlogging-sensitive Brassica napus L. (G218) were provided by the National Oil Crops Improvement Center in Hunan. Their tolerance to waterlogging stress was identified in our previous study [22]. They were sown in October 2021 at the Yuyuan Base of Hunan Agricultural University (28°12’ N, 112°59’E). When the seedlings reached the five-leaf, they were subjected to waterlogging stress for six days. Flooding was carried out in the field, with the water level exceeding the soil surface by approximately two centimeters. Three plants from each material were selected for sampling of roots and leaves, and this process was repeated three times, with normal field-grown plants during the same period used as controls.

Physiological index determination

Fresh leaves and roots of rapeseed weighing 0.1 g were taken to determine the contents of soluble sugars, proline (Pro), malondialdehyde (MDA), and hydrogen peroxide (H2O2), as well as the activities of peroxidase (POD) and superoxide dismutase (SOD). All physiological indices were determined using reagent kits produced by Sangon Biotech Co. (Shanghai, China) according to the instructions. The contents of oleic acid and linoleic acid were detected by gas chromatography [48], and the oil content and protein content were detected by near-infrared reflectance spectroscopy [49].

Cell safranin O - fast green staining

The root segments were cut to a length of approximately 1 mm, and leaf sections were cut to a size of approximately 1 mm × 1 mm. They were soaked in 70% FAA fixative for 24 h. The FAA fixative was prepared by mixing 70% ethanol, glacial acetic acid, and formaldehyde in a ratio of 90: 5: 5. Dehydration was performed using an ethanol gradient (30%, 50%, 70%, 90%, and 100%), followed by transparency using xylene. The samples were embedded in paraffin at 60 °C using a LEICA SM 2010 R microtome (Wetzlar, Germany) to obtain 8 μm thick sections. The fully dried slides were dewaxed in xylene (30 min) and ethanol (30 min) until water was reached. They were stained with hematoxylin for three minutes, rinsed with tap water, differentiated in acid alcohol for 15 s, rinsed again with tap water, stained with 1% safranin O solution for three minutes, quickly rinsed with 1% acetic acid, stained with 0.5% fast green solution for three minutes, rinsed with 95% ethanol, made transparent with xylene, mounted with neutral gum, and observed under a LEICA ICC50 W optical microscope (Wetzlar, Germany) to examine the root and leaf structures [50].

Transmission electron microscopy observation

Similarly, the root segments were cut to a length of approximately 1 mm, and leaf sections were cut to a size of approximately 1mm2. They were first fixed with electron microscopy fixative (3% glutaraldehyde) at 4 °C for 24 h, followed by fixation with 1% osmium tetroxide. Subsequently, the samples were dehydrated stepwise with acetone, embedded in epoxy resin, sectioned using a LEICA EM UC7 ultramicrotome (Wetzlar, Germany), stained with lead citrate and uranyl acetate for five minutes each, and finally observed under a JEM 1200 EX transmission electron microscope (Tokyo, Japan) [50].

Quantitative real‑time PCR (qRT‑PCR) analysis

The relative transcription levels of three genes related to anaerobic respiration and three genes related to flavonoid biosynthesis were analyzed by qRT-PCR. Primers were designed on NCBI (https://www.ncbi.nlm.nih.gov/) and listed in Table 2. The RNA was extracted from the samples (G218 and G230), and first-strand cDNA was synthesized by employing TransScript First-Strand cDNA Synthesis SuperMix (TransGene, AT301-02) in accordance with the manufacturer’s instructions. qRT-PCR was conducted using PerfectStart® Green qPCR SuperMix (TransGene, AQ601-02) as per the manufacturer’s instructions. In this study, qRT-PCR was carried out with three biological replicates, and each replicate included three technical repeats. The relative expression levels were calculated according to the method described by 2−∆∆CT [51].

Table 2 Primer used for qRT-PCR
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Exogenous catechin treatment

G230 and G218 were grown in pots, and waterlogging stress was applied for six days at the seedling stage (five leaves). Before the treatment, the plants were sprayed with epicatechin at a concentration of 5µmol/L on the leaf surface. The experiment was repeated three times, and the epicatechin reagent was purchased from Coolaber (Beijing, China).

Statistical analyses

Analysis of data collected from physiological experiments and qRT-PCR using Microsoft Office Excel. Significance analysis was performed using one-way analysis of variance (ANOVA) and Duncan’s multiple range test in SPSS Statistics 22.0 software, where P < 0.05 indicated a significant difference. All values are represented as the mean of three biological replicates ± standard deviation (SD).

Data availability

Data is provided within the manuscript or supplementary information files.

Abbreviations

WS:

The waterlogging stress treatment

CK:

The control check

EGCG:

Epigallocatechin gallate

P:

Phloem

Xy:

Xylem

Sx:

Secondary xylem

VE:

Vessel

N:

Nucleus

CW:

Cell wall

Ch:

Chloroplast

Mi:

Mitochondria

S:

Starch granules

GL:

Grana lamella

OG:

Osmiophilic granules

V:

Vacuole

PE:

Peroxisome

EC:

Epicatechin

MDA:

Malondialdehyde

Pro:

Proline

POD:

Peroxidase

SOD:

Superoxide dismutase

H2O2 :

Hydrogen peroxide

FAA:

Formalin-Aceto-Alcohol

SD:

Standard deviation

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Funding

This research was funded by the Hunan Agriculture Research System (HARS-03).

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Authors and Affiliations

  1. College of Agriculture, Hunan Agricultural University, Changsha, 410128, China

    Bo Hong, Bingqian Zhou, Dongfang Zhao, Li Liao, Tao Chang, Xuepeng Wu, Junjie Wu, Mingyao Yao, Hu Chen, Jiajun Mao, Chunyun Guan & Mei Guan

  2. Hunan Branch of National Oilseed Crops Improvement Center, Changsha, 410128, China

    Bo Hong, Bingqian Zhou, Dongfang Zhao, Li Liao, Tao Chang, Xuepeng Wu, Junjie Wu, Mingyao Yao, Hu Chen, Jiajun Mao, Chunyun Guan & Mei Guan

  3. Southern Regional Collaborative Innovation Center for Grain and Oil Crops in China, Changsha, 410128, China

    Chunyun Guan & Mei Guan

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  1. Bo Hong
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Contributions

BH, CG, and MG designed the experiment. BH undertook the main experimental work and wrote the manuscript. BH and BZ analyzed the data. BZ, DZ, LL, TC, XW, JW, MY, HC and JM assisted with experiments and rapeseed material planting. MG helped revise the manuscript. All authors reviewed the manuscript.

Corresponding authors

Correspondence to Chunyun Guan or Mei Guan.

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Hong, B., Zhou, B., Zhao, D. et al. Yield, cell structure and physiological and biochemical characteristics of rapeseed under waterlogging stress. BMC Plant Biol 24, 941 (2024). https://doi.org/10.1186/s12870-024-05599-z

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BMC Plant Biology

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