Next Article in Journal
Genome-Wide Identification, Expression and Response to Estrogen of Vitellogenin Gene Family in Sichuan Bream (Sinibrama taeniatus)
Previous Article in Journal
Hydrogen-Rich Alkaline Water Supplementation Restores a Healthy State and Redox Balance in H2O2-Treated Mice
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
IJMS
Volume 25
Issue 12
10.3390/ijms25126738
ijms-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Article

Adaptation of the Invasive Plant Sphagneticola trilobata to Flooding Stress by Hybridization with Native Relatives

by
Qilei Zhang
1,2,
Guangxin Chen
1,
Weiqian Ke
1 and
Changlian Peng
1,*
1
Guangzhou Key Laboratory of Subtropical Biodiversity and Biomonitoring, Guangdong Provincial Key Laboratory of Biotechnology for Plant Development, School of Life Sciences, South China Normal University, Guangzhou 510631, China
2
Research Institute of Tropical Forestry, Chinese Academy of Forestry, Guangzhou 510520, China
*
Author to whom correspondence should be addressed.
Int. J. Mol. Sci. 2024, 25(12), 6738; https://doi.org/10.3390/ijms25126738
Submission received: 28 April 2024 / Revised: 8 June 2024 / Accepted: 17 June 2024 / Published: 19 June 2024
(This article belongs to the Section Molecular Plant Sciences)
Browse Figures
Versions Notes

Abstract

:
Hybridization is common between invasive and native species and may produce more adaptive hybrids. The hybrid (Sphagneticola × guangdongensis) of Sphagneticola trilobata (an invasive species) and S. calendulacea (a native species) was found in South China. In this study, S. trilobata, S. calendulacea, and Sphagneticola × guangdongensis were used as research materials to explore their adaptability to flooding stress. Under flooding stress, the ethylene content and the expression of key enzyme genes related to ethylene synthesis in Sphagneticola × guangdongensis and S. calendulacea were significantly higher than those in S. trilobata. A large number of adventitious roots and aerenchyma were generated in Sphagneticola × guangdongensis and S. calendulacea. The contents of reactive oxygen species and malondialdehyde in Sphagneticola × guangdongensis and S. calendulacea were lower than those in S. trilobata, and the leaves of S. trilobata were the most severely damaged under flooding stress. The results indicate that hybridization catalyzed the tolerance of Sphagneticola × guangdongensis to flooding stress, and the responses of Sphagneticola × guangdongensis to flooding stress were more similar to that of its native parent. This suggests that hybridization with native relatives is an important way for invasive species to overcome environmental pressure and achieve invasion.

1. Introduction

Biological invasions threaten ecosystem function and biological diversity and have long-term ecological consequences [1]. At the same time, it is common for invasive species to hybridize with native species during biological invasion, which may produce more adaptive hybrids [2,3,4]. For example, Spartina angelica is a hybrid species produced by natural hybridization between S. altermiflora and S. marime, and its invasive ability is stronger than that of its parents [4,5]. Hybridization is a mechanism of invasive evolution in exotic plant species that can generate new hybrids that spread wider than their parents. For example, the invasive species Helianthus paradoxes is a hybrid produced by natural hybridization between H. annuus and H. petiolaris [6]. Hybridization is particularly important under constantly changing environmental conditions [7]. Heterosis is the result of the non-additive phenotypic expression of one or more traits, which may be regulated by epigenetics and genetics. Under environmental pressure, heterosis may lead to hybrid varieties with extreme phenotypes, exhibiting higher adaptability than their parents [8].
With global warming, frequent outbreaks of extreme weather, such as heavy rainfall and floods, have led to long-term flooding in some areas [9,10]. Water is one of the essential environmental factors for plants, but flooding is detrimental to the growth and development of terrestrial plants. Its distribution in the environment regulates the distribution, diversity, and succession characteristics of vegetation [11].
Most terrestrial plants are susceptible to damage under flooding events. The damage caused by flooding to plants is mainly due to a significant decrease in the diffusion rate of gases in water. Thus, the gas exchange between the submerged plant tissue and the environment is hindered. This affects the availability of CO2 and O2, reduces the production of photosynthetic products, and ultimately leads to plant mortality [12,13]. In plants, floods affect the stomatal conductance, leading to a decrease in the net photosynthetic rate (Pn) of leaves. The decrease in the net photosynthetic rate may be due to the decrease in the CO2 concentration caused by changes in the stomatal aperture [14,15]. The decrease in the Pn alters the flow of electrons along the electron transport chain, leading to the production of more reactive oxygen species (ROS). Proteins, lipids, and nucleic acids will be destroyed due to the increase in ROS activity, leading to further reductions in the Pn [16].
The roots of plants are the most susceptible organ to flooding. After the soil is covered by floods, the oxygen content in it decreases, causing the plant roots to be in an anaerobic environment [15]. Under hypoxic conditions, the absorption rate of minerals by the root system decreases, which cannot meet the growth needs of the aboveground parts of plants, resulting in slow plant growth [17]. Flooding not only alters soil compaction and microbial composition around roots but also intensifies competition among root microorganisms for nutrients and oxygen [18]. Root hypoxia causes energy imbalance, excessive production of ROS, and nitric oxide in the root system, thereby damaging the root tissue [19]. Therefore, the damage of flooding to plants is multifaceted and can damage the normal development and function of root systems. Ultimately, this leads to the loss of mineral absorption capacity in the root system, affecting the growth of the entire plant [20,21].
Plants have developed adaptive strategies in flooded environments, which have improved their tolerance to flooding stress. Stimulating growth to escape flooded conditions is one strategy; in order to obtain sufficient carbon dioxide, light, and oxygen, the upper stems and leaves of plants are exposed to the water surface [22]. Flood-tolerant plants have adopted a strategy of hypoxia quiescence syndrome, which extends their survival time in water by maintaining lower energy and carbon consumption [23]. Faced with flooding, adaptive changes occur in the roots and stems of plants, thereby improving their tolerance to flooding. For example, the formation of aerenchyma in roots and stems facilitates gas flow, accelerates stem elongation, and promotes adventitious root growth [24,25]. Flooding stress stimulates the synthesis and accumulation of ethylene, leading to the formation of aerenchyma, and interconnecting plant bodies form a unified entity. In addition, ethylene also promotes the formation of adventitious roots [26,27], which replaces the primary roots that die from hypoxia and obtains more nutrients and oxygen. Additionally, the antioxidant capacity is enhanced under flooding stress to remove excess ROS, which reduces damage to plants [28].
Sphagneticola trilobata (L.) Pruski is an invasive plant species in South China that originated in South and Central America. A hybrid, Sphagneticola × guangdongensis (Asteraceae, Heliantheae), found in South China, is the hybrid of S. trilobata and its native relative S. calendulacea (L.) Pruski [29,30]. The growth potential of the hybrid species Sphagneticola × guangdongensis is higher than that of the native species S. calendulacea and comparable to the invasive species S. trilobata, and its light energy utilization efficiency is higher than that of both the invasive and native species [29]. Under N deposition, the competitiveness of Sphagneticola × guangdongensis is similar to that of the invasive species and more sensitive [31]. We previously reported that the tolerance of Sphagneticola × guangdongensis to cadmium was stronger than its parents [32,33], and its tolerance to drought stress was higher than the native species and lower than the invasive species [34,35]. However, the tolerance level of Sphagneticola × guangdongensis to flooding stress is largely unknown. The aim of this study was to investigate the tolerance of the hybrid species Sphagneticola × guangdongensis to flooding stress and explore whether the invasive species S. trilobata could improve its adaptability to flooding stress by hybridizing with the native species S. calendulacea.

2. Results

2.1. Phenotypic Characteristics

By observing the phenotypic changes in Sphagneticola × guangdongensis and its parents under water flooding stress (Figure 1), it was found that the leaves of both Sphagneticola × guangdongensis and its two parents exhibited decay or shedding with prolonged flooding. However, the effects of flooding stress on the three species were different, and the invasive species S. trilobata suffered the most severe damage. After 2 days of flooding stress, necrotic spots were observed on the young leaves of the invasive species S. trilobata (Figure 1f). However, the young leaves of the hybrid species Sphagneticola × guangdongensis and the native species did not show necrotic spots (Figure 1e,g).

2.2. Accumulation of ROS and Changes in Photosynthetic Capacity

Flooding stress led to membrane lipid peroxidation, a large amount of production and accumulation of ROS, and an increase in electrolyte leakage rates. H2O2 was detected with DAB staining, and O2– was detected with NBT staining at 12 days after flooding stress. The highest levels of H2O2 and O2– were detected in the leaves of the invasive species S. trilobata (Figure 2b,d). The degree of lipid peroxidation in cell membranes can be reflected by their MDA content. Flooding stress caused a significant increase in the MDA content in the leaves (F = 41.68; df = 5, 24). As shown in Figure 2e, the content of MDA in the invasive species S. trilobata was the highest, while it was lower in Sphagneticola × guangdongensis and S. calendulacea. The MDA content in the invasive species was significantly higher than that in Sphagneticola × guangdongensis (p < 0.01) and the native species (p < 0.01) but not significantly different between Sphagneticola × guangdongensis and the native species (p = 0.74). Sphagneticola × guangdongensis and S. calendulacea showed lower electrolytic leakage than S. trilobata under flooding stress (Figure 2f) (F = 93.98; df = 5, 24).
During the flooding, the Fv/Fm and ETR values in the leaves of Sphagneticola × guangdongensis and its parents gradually decreased (Figure 2g,h). After 6 days of flooding, the Fv/Fm and ETR values were the lowest in the leaves of the invasive species (S. trilobata), second lowest in the hybrid species Sphagneticola × guangdongensis, and highest in the native species S. calendulacea. The Pn value gradually decreased under flooding stress. The Pn was higher in Sphagneticola × guangdongensis than in S. trilobata after 9 d of flooding (Figure 2i).
The contents of chlorophyll and Rubisco are closely related to the photosynthesis of plant leaves, and they decreased after 12 days of flooding stress (Figure 2j), which is consistent with the results of the Pn. Western blotting analysis was carried out on a Rubisco large subunit (RubL) (Figure 2k), and it could not be detected in the invasive species S. trilobata. Compared to the control, flooding stress significantly reduced the increase in biomass (F = 470.82; df = 5, 24; p < 0.05). Under flooding stress, the increase in the biomass of S. trilobata was significantly lower than that of Sphagneticola × guangdongensis (p = 0.014) and S. calendulacea (p = 0.002). There was no significant difference in the biomass changes between Sphagneticola × guangdongensis and S. calendulacea (p = 0.406). However, without flooding stress, the magnitude of the biomass increase was significantly larger in the invasive species, compared to that of the Sphagneticola × guangdongensis and the native species (p < 0.01). These results imply that the invasive species S. trilobata suffered the most severe damage under flooding stress (Figure 2l).

2.3. Adventitious Roots and Aerenchyma

Adventitious roots were observed in the hybrid species Sphagneticola × guangdongensis and the native species S. calendulacea under flooding stress for 5 h and 24 h but did not appear in the invasive species S. trilobata (Figure 3a). After 12 days of flooding, there were differences in the aerenchyma, with a large amount of aerenchyma present in Sphagneticola × guangdongensis and the native species (Figure 3b). The results showed that Sphagneticola × guangdongensis and the native species produced adventitious roots in every plant after 3 days under flooding stress, while the number of plants of the invasive species that produced adventitious roots reached its maximum after 4 days of flooding stress, at only about 20% (Figure 3c). Compared to the group not under flooding, flooding stress significantly reduced the number of stem nodes (Kruskal–Wallis test, F = 46.99, df = 5, p < 0.05; Mann–Whitney post hoc test), with the largest decrease observed in the invasive species (Figure 3d). Under flooding stress, the number of stem nodes in S. trilobata was lower than that in Sphagneticola × guangdongensis (p = 0.111) and S. calendulacea (p = 0.054). There was no significant difference in the number of stem nodes between Sphagneticola × guangdongensis and S. calendulacea (p = 0.739). However, without flooding stress, the number of stem nodes was the highest in the invasive species S. trilobata, compared to that in Sphagneticola × guangdongensis (p = 0.422) and the native species (p = 0.258). However, the stem node lengths of Sphagneticola × guangdongensis and the native species significantly increased under flooding stress (Kruskal–Wallis test, F = 53.16, df = 5, p < 0.05; Mann–Whitney post hoc test), and there was no significant change in the stem node length of the invasive species (Figure 3e) (p = 0.969).

2.4. Expression Levels of Ethylene Synthesis and Transduction-Related Genes

After flooding, the ethylene contents of the hybrid species Sphagneticola × guangdongensis (p < 0.01) and the native species S. calendulacea (p < 0.01) increased significantly, compared to the invasive species S. trilobata, but there was no significant difference between Sphagneticola × guangdongensis and the native species (Figure 4a) (F = 149.98; df = 2, 6; p = 0.644). Transcriptome analysis was conducted to investigate the expression of genes involved in ethylene synthesis and the signal transduction pathways under waterlogging stress. The expression levels of key enzyme genes for ethylene synthesis and positive regulatory genes in the ethylene signaling pathway were upregulated, with the expression levels of Sphagneticola × guangdongensis and the native species higher than those of the invasive species. The expression levels of negative regulatory genes in the ethylene signaling pathway were downregulated, with the expression levels of Sphagneticola × guangdongensis and the native species significantly lower than those of the invasive species (Figure 4b). The aminocyclopropane-1-carboxylic acid synthase gene (ACS) and aminocyclopropane-1-carboxylic acid oxidase gene (ACO) are the key enzymatic genes in ethylene biosynthesis, and the changes in their expression levels were consistent with the changes in the ethylene content. The ethylene response gene (ETR) and the ethylene insensitive3 gene (EIN3) are key enzyme genes for negative and positive regulation in ethylene signal transduction, respectively. The relative expression levels of ACS, ACO, ETR, and NIE3 genes detected using real-time PCR were consistent with the transcriptome results (Figure 4c–f).

3. Discussion

The tolerance of the hybrid species Sphagneticola × guangdongensis and the native species S. calendulacea to flooding stress was stronger that of the invasive species S. trilobata. Several authors have reported that hybridization during plant invasion may produce more adaptable hybrid species [4,5,36]. For example, the hybridization between the native species Spartina foliosa and the invasive species S. densiflora enhanced the adaptability of the hybrid species to salt and flooding stress [7]. In our previous research, the tolerance of Sphagneticola × guangdongensis to cadmium and drought stress was inconsistent with the tolerance of Sphagneticola × guangdongensis to flooding stress in this study [32,33,34,35]. Ni et al. [31] found that the hybrid species Sphagneticola × guangdongensis was more sensitive to nitrogen deposition than the invasive species. The tolerance of Sphagneticola × guangdongensis to low temperature and low light was lower than that of the invasive species S. trilobata and the native species S. calendulacea [37]. The results of this study indicate that the hybrid species Sphagneticola × guangdongensis had stronger resistance to flooding stress than the invasive species S. trilobata and was closer to the native species S. calendulacea. As the flooding time continued, the leaves of both Sphagneticola × guangdongensis and its parents showed varying degrees of yellowing and shedding, with the invasive species suffering the most severe damage. After 2 days of flooding, necrotic spots appeared on the young leaves of the invasive species (Figure 1f). This implies that the tolerance of the invasive species was the weakest to flooding stress, while Sphagneticola × guangdongensis and the native species had stronger resistance to flooding stress. Flooding stress led to plant leaf decay and shedding, which was confirmed in other studies, and the species with stronger resistance suffered less damage on their leaves [38].
The net photosynthetic rate of the invasive species S. trilobata decreased the fastest, that of the native species S. calendulacea decreased the slowest, and that of the hybrid species Sphagneticola × guangdongensis decreased at a rate between its parents under flooding stress. Photosynthesis is the foundation of plant growth, and its changes under flooding stress reflect the degree of damage to plants [33]. Under flooding stress, the net photosynthetic rate of Sphagneticola × guangdongensis and its parents gradually decreased (Figure 2i), indicating that flooding stress caused damage to the plants [39]. Among them, the invasive species had the fastest decline rate, while Sphagneticola × guangdongensis and the native species had higher net photosynthetic rates than the invasive species, indicating that the invasive species suffered the most severe damage. Chlorophyll and Rubisco are the main substances responsible for light energy absorption and carbon fixation in photosynthesis, and changes in the chlorophyll and Rubisco can directly affect the net photosynthetic rate [40]. Flooding stress led to the degradation of chlorophyll and Rubisco in the plant leaves, resulting in a decrease in their contents. In this experiment, the contents of chlorophyll and Rubisco large subunits significantly decreased after flooding stress, with the highest contents being in the native species and the lowest being in the invasive species (Figure 2j,k). Previous studies also found decreases in the chlorophyll and Rubisco contents of Arabidopsis and Prunus leaves under flooding stress [13,28].
The invasive species S. trilobata suffered the most serious oxidative damage from flooding stress, compared to the hybrid species Sphagneticola × guangdongensis and the native species S. calendulacea. When the plants were subjected to flooding stress, the accompanying oxidative stress led to an increase in the content of ROS, and the accumulation of a large amount of ROS is toxic to plants [13,28,41]. In this study, the invasive species accumulated more H2O2 and O2– than Sphagneticola × guangdongensis and the native species (Figure 2c,d). As toxic substances, H2O2 and O2– can cause damage to plants by attacking their cell membranes and disrupting their biomolecules, among other means [41]. The degree of damage to membrane lipids can be indirectly reflected by the MDA content, which is the product of membrane lipid peroxidation. In this study, the MDA content in the leaves of the hybrid species Sphagneticola × guangdongensis and the native species S. calendulacea under flooding was lower than that of the invasive species, indicating that the tolerance of the invasive species was the weakest to flooding stress. Cell membrane damage led to higher ion leakage [42]. Under flooding stress, the cell membrane electron permeability of the invasive species was significantly higher than that of Sphagneticola × guangdongensis and the native species, but there was no significant difference between Sphagneticola × guangdongensis and the native species (Figure 2f). The tolerance of plants under flooding stress is related to the stability of their membrane structure. The MDA content and ion leakage are lower in plants with a strong tolerance [42,43,44]. These results imply that Sphagneticola × guangdongensis and the native species have greater tolerance to flooding stress than the invasive species.
The adaptive strategies of the hybrid species Sphagneticola × guangdongensis and the native species S. calendulacea under flooding stress were more effective than those of the invasive species S. trilobata. One of the critical strategies for plants to adapt to flooding stress is the formation of adventitious roots. The replacement of the malfunctioning primary roots by adventitious roots increases the plant’s access to oxygen and nutrients and enhances its tolerance to flooding stress [45]. The results showed that under flooding stress, Sphagneticola × guangdongensis and the native species formed a large number of adventitious roots quickly, while nearly 80% of the invasive plants did not form adventitious roots (Figure 3c). Aerenchyma is another important strategy for adapting to flooding stress, and its formation connects plants and transport oxygen obtained from the upper part downwards. Furthermore, it reduces the number of cells and the amount of oxygen consumption. After flooding, Sphagneticola × guangdongensis and the native species formed more aerenchyma than the invasive species (Figure 3b), which improves plant resistance under flooding stress [40]. These results suggest that the resistance of Sphagneticola × guangdongensis and the native species to flooding stress is stronger than that of the invasive species.
The formation of aerenchyma and adventitious roots was significantly positively correlated with changes in the ethylene content. Ethylene hinders the downward transport of auxin, promoting the formation of adventitious roots [46], and it increases cellulase activity and promotes the formation of aerenchyma [27]. The results showed that the increase in the ethylene content in Sphagneticola × guangdongensis and the native species was significantly higher than that in the invasive species after flooding stress (Figure 4a). Through transcriptome sequencing and real-time quantitative PCR analysis, it was found that the relative expression levels of the key enzyme genes ASC and ACO were significantly upregulated, which was positively correlated with ethylene synthesis [47,48], and the relative expression levels of Sphagneticola × guangdongensis and the native species were significantly higher than those of the invasive species. These genes, which are positively regulated in ethylene signal transduction, were upregulated, and their trends were consistent with those of the key enzyme genes in ethylene synthesis. The expression levels of the negative regulatory genes were downregulated, and the downregulation amplitude of the invasive species was the smallest (Figure 4b–f). The changes in gene expression were consistent with the changes in the ethylene content.

4. Materials and Methods

4.1. Plant Materials

The plant materials of S. trilobata, S. calendulacea, and their hybrid species Sphagneticola × guangdongensis were collected from the South China Botanical Garden, which is affiliated with the Chinese Academy of Sciences in Guangzhou, China [29]. These plant materials underwent a process of asexual propagation for cultivation. The stem with removed leaves was cut into about 10 cm and contained two pairs of buds for each piece. Subsequently, we placed the segments in an opaque container containing tap water and waited for them to take root and grow new leaves. Then, we transplanted the seedlings into growth substrate (a mixture of red soil and sand at a 3:1 ratio, v/v) in plastic pots. The seedlings exhibiting consistent growth after 28 days were chosen for the experiment. These selected seedlings were then divided into two groups: one group was subjected to flooding, while the other served as a non-flooding control. The plants in the flooding treatment group were placed individually into separate 100 L plastic containers filled with tap water. The plants in the flooding treatment were completely submerged in the tap water, with the water surface positioned 5 cm above the top of the plants. In contrast, the control treatment involved non-submerged plants that were irrigated daily. Five replications of each experimental unit, with 10 plants per treatment, were set. Samples with more than 5 biological replicates were taken from five experimental units separately, while samples with fewer than 5 biological replicates were randomly selected from five experimental units randomly.

4.2. Net Photosynthetic Rate and Chlorophyll Fluorescence Parameters

The Li-6800 photosynthesis measuring instrument (Li-Cor, Lincoln, NE, USA) was used to measure the leaf photosynthesis rate (Pn) using the method reported by Zhang et al. [49]. We selected one plant for each experimental unit, totaling five plants.
The chlorophyll fluorescence parameters were measured using a chlorophyll fluorescence imaging system (Technologica, Colchester, UK). Plant leaves were adapted at 900 μmol m–2 s–1 for 5 min, and then we determined the maximum fluorescence (Fm′) and steady fluorescence (Fs). The maximum fluorescence (Fm) and minimum fluorescence (Fo) were recorded after 30 min of dark adaptation under a 6000 μmol m–2 s–1 saturating pulse. The value of the effective quantum yield of the PSII (ΦPSII), the electron transfer rate (ETR), and the maximum photochemical efficiency (Fv/Fm) were calculated according to the methods in [50,51,52]. We selected one plant for each experimental unit, totaling five plants.

4.3. Rubisco Protein Western Blotting

Rubisco protein determination was performed using the method reported by Zhang et al. [49], with Bio-Rad 12% precast gradient gels. The Rubisco protein was detected with the anti-Rubisco antibody (Bioss, Beijing, China). Antibodies were diluted at 1:1000 in 5% non-fat milk in TBS-T.

4.4. Measurement of Electrolyte Leakage Rates and Malondialdehyde

A method described previously [53] was used to measure the electrolyte leakage rates. The FG3-ELK conductivity meter (Mettler Toledo, Zurich, Switzerland) was used to test the conductivity of the solution. The percentage of initial conductivity to the total conductivity was used to represent the rate of ion leakage. The malondialdehyde (MDA) content was measured according to the method published by Sun et al. [37]. We selected one plant for each experimental unit, totaling five plants.

4.5. Histochemical Staining

Nitro blue tetrazolium (NBT) histochemical staining was used to determine the superoxide anions (O2–), and diaminobenzidine (DAB) histochemical staining was used to determine the hydrogen peroxide (H2O2) [54].

4.6. Anatomical Analysis

We washed the adventitious roots of the plants in tap water and then cut them into 0.5 cm pieces using a blade. We soaked the cut roots in a centrifuge tube containing formalin and sank the roots to the bottom of the centrifuge tube by vacuum pumping. Dehydration was carried out using different concentrations of ethanol. Technovit 7100 resin (Wehrheim, Germany) was used to infiltrate the fixed roots, and then the fixed roots were embedded. Afterwards, they were stained with safranin (1%) and recorded using a microscope (Olympus CX30, Tokyo, Japan) after the cross-sections of the roots were sectioned [39].

4.7. Ethylene Measurement

The ethylene was measured as previously described [55]. In summary, the plants grew in a transparent enclosed container under flooding stress for 2 days. A 100 mL gas sample was collected, and the ethylene content was detected using gas chromatography (Varian CP-3800, Agilent Corporation, Santa Clara, CA, USA). We selected 3 plants randomly from the five experimental units.

4.8. Transcriptome Sequencing and Gene Expression Analysis

The method reported by Zhang et al. [35] was used to analyze the gene expression. The method described by Livak and Schmittgen [56] was used to analyze the genes’ relative expression levels. We selected 3 plants randomly from the five experimental units. The GAPDH gene was used as an internal reference, and the primer pairs were 5′-GGCTCGACTCGGCATATTCT-3′ (forward) and 5′-CGGCTGCCTTTGGTCTATGT-3′ (reverse). The primer pairs for the ethylene synthesis-related gene aminocyclopropane-1-carboxylic acid synthase gene (ACS) were 5′-GAGTTCGGTTAGCCCGTAGG-3′ (forward) and 5′-CGTTGTGGTCTCGTCATCCA-3′ (reverse), and for aminocyclopropane-1-carboxylic acid oxidase (ACO), they were 5′-TAGAGAAGCTGGCAGAGGGT-3′ (forward) and 5′-TGGCACGTCAATCCACTTGT-3′ (reverse). The primer pairs for ethylene signal transduction-related gene ethylene response (ETR) were 5′-CGTCGTTTGGCATCTGGTTC-3′ (forward) and 5′-TTTCTGGAGTTTGGAGGGCA-3′ (reverse), and for the ethylene insensitive3 gene (EIN3), they were 5′-CCAAAGCAGGATGGGTCTGT-3′ (forward) and 5′-AGAGGGCATCCTTGACTCCT-3′ (reverse). RNA sequencing data are available in the Gene Expression Omnibus (GEO) database under accession number SUB13842716.

4.9. Statistical Analysis

SPSS Statistics 19.0 (IBM, Armonk, NY, USA) was used for the statistical analysis. The data were subjected to a normal distribution test, and for data that conformed to a normal distribution, one-way analysis of variance was used. Duncan’s post hoc test was used for pairwise comparison. For data that did not conform to a normal distribution, the Kruskal–Wallis method was used, and the Mann–Whitney post hoc test was used for pairwise comparison. The significance was set as p < 0.05. SigmaPlot 12.5 (Systat Software Inc., Richmond, VA, USA) was used to conduct linear regression analysis and to plot the data. The values were expressed as the means ± standard errors.

5. Conclusions

This study indicated that hybridization with the native species S. calendulacea catalyzed the tolerance of the hybrid species Sphagneticola × guangdongensis to flooding stress. Under flooding stress, Sphagneticola × guangdongensis and the native species significantly upregulated the synthesis and accumulation of ethylene, promoted the formation of adventitious roots and aerenchyma, and improved their resistance to flooding stress, while the resistance in the invasive species was the weakest (Figure 5). Therefore, flooding stress may be a limiting factor for the spread and distribution of the invasive species S. trilobata, which may be overcome by hybridization with native species [57]. From a genetic perspective, this could be a method of gene invasion by spreading the genes of an invasive species through hybridization with a native species. Hybridization with native relatives is an important method for the successful invasion of invasive species.

Author Contributions

C.P. proposed the project. C.P. and Q.Z. designed the experiments. Q.Z., W.K. and G.C. performed the experiments. Q.Z. analyzed the data and wrote the manuscript. All authors have read and agreed to the published version of the manuscript.

Funding

This work was supported by the National Science Foundation of China (32171493, 31870374) and the Guangdong Basic and Applied Basic Research Foundation (2022A1515110960).

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Data are contained within the article.

Conflicts of Interest

The authors declare no conflicts of interest.

References

  1. Mahood, A.L.; Jones, R.O.; Board, D.I.; Balch, J.K.; Chambers, J.C. Interannual climate variability mediates changes in carbon and nitrogen pools caused by annual grass invasion in a semiarid shrubland. Glob. Chang. Biol. 2022, 28, 267–284. [Google Scholar] [CrossRef]
  2. Bock, D.G.; Baeckens, S.; Pita-Aquino, J.N.; Chejanovski, Z.A.; Michaelides, S.N.; Muralidhar, P.; Lapiedra, O.; Park, S.; Menke, D.B.; Geneva, A.J.; et al. Changes in selection pressure can facilitate hybridization during biological invasion in a Cuban lizard. Proc. Natl. Acad. Sci. USA 2021, 118, e2108638118. [Google Scholar] [CrossRef]
  3. Qiao, H.; Liu, W.; Zhang, Y.; Zhang, Y.; Li, Q.Q. Genetic admixture accelerates invasion via provisioning rapid adaptive evolution. Mol. Ecol. 2019, 28, 4012–4027. [Google Scholar] [CrossRef]
  4. Xia, L.; Zhao, H.; Yang, W.; An, S.Q. Genetic diversity, ecotype hybrid, and mixture of invasive Spartina alterniflora loisel in Coastal China. Clean-Soil Air Water 2015, 43, 1672–1681. [Google Scholar] [CrossRef]
  5. Abbott, R.J.; Brennan, A.C.; James, J.K.; Forbes, D.G.; Hegarty, M.J.; Hiscock, S.J. Recent hybrid origin and invasion of the British Isles by a self-incompatible species, Oxford ragwort (Senecio squalidus L., Asteraceae). Biol. Invasions 2009, 11, 1145–1158. [Google Scholar] [CrossRef]
  6. Lexer, C.; Welch, M.E.; Durphy, J.L.; Rieseberg, L.H. Natural selection for salt tolerance quantitative trait loci (QTLs) in wild sunflower hybrids: Implications for the origin of Helianthus paradoxus, a diploid hybrid species. Mol. Ecol. 2003, 12, 1225–1235. [Google Scholar] [CrossRef]
  7. Gallego-Tévar, B.; Grewell, B.J.; Drenovsky, R.E.; Castillo, J.M. Transgressivity in key functional traits rather than phenotypic plasticity promotes stress tolerance in a hybrid cordgrass. Plants 2019, 8, 594. [Google Scholar] [CrossRef]
  8. Hamilton, J.A.; Royauté, R.; Wright, J.W.; Hodgskiss, P.; Ledig, F.T. Genetic conservation and management of the California endemic, Torrey pine (Pinus torreyana Parry): Implications of genetic rescue in a genetically depauperate species. Ecol. Evol. 2017, 7, 7370–7381. [Google Scholar] [CrossRef]
  9. Sprunger, C.D.; Lindsey, A.; Lightcap, A. Above- and belowground linkages during extreme moisture excess: Leveraging knowledge from natural ecosystems to better understand implications for row-crop agroecosystems. J. Exp. Bot. 2023, 74, 2845–2859. [Google Scholar] [CrossRef]
  10. Tanoue, M.; Hirabayashi, Y.; Ikeuchi, H. Global-scale river flood vulnerability in the last 50 years. Sci. Rep. 2016, 6, 36021. [Google Scholar] [CrossRef]
  11. Campbell, D.; Keddy, P. The roles of competition and facilitation in producing zonation along an experimental flooding gradient: A tale of two tails with ten freshwater marsh plants. Wetlands 2022, 42, 1–14. [Google Scholar] [CrossRef]
  12. Zhang, Y.; Li, Z.; Ge, W.; Wang, J.; Guo, X.; Wang, T.; Li, W. Assessment of the impact of floods on terrestrial plant biodiversity. J. Clean. Prod. 2022, 339, 130722. [Google Scholar] [CrossRef]
  13. Zhou, W.; Chen, F.; Meng, Y.; Chandrasekaran, U.; Luo, X.; Yang, W.; Shu, K. Plant waterlogging/flooding stress responses: From seed germination to maturation. Plant Physiol. Biochem. 2020, 148, 228–236. [Google Scholar] [CrossRef]
  14. Langan, P.; Bernád, V.; Walsh, J.; Henchy, J.; Khodaeiaminjan, M.; Mangina, E.; Negrão, S. Phenotyping for waterlogging tolerance in crops: Current trends and future prospects. J. Exp. Bot. 2022, 73, 5149–5169. [Google Scholar] [CrossRef]
  15. Leeggangers, H.A.; Rodriguez-Granados, N.Y.; Macias-Honti, M.G.; Sasidharan, R. A helping hand when drowning: The versatile role of ethylene in root flooding resilience. Environ. Exp. Bot. 2023, 213, 105422. [Google Scholar] [CrossRef]
  16. Yu, L.; Zhang, Q.; Lu, L.; Gao, H.; Liu, Q.; Liu, Y.; Yang, C.; Peng, C. The role of ascorbic acid in rice leaf senescence and photo-carbon imbalance. Funct. Plant Biol. 2020, 47, 263–278. [Google Scholar] [CrossRef]
  17. Ren, B.; Zhang, J.; Dong, S.; Liu, P.; Zhao, B. Root and shoot responses of summer maize to waterlogging at different stages. Agron. J. 2016, 108, 1060–1069. [Google Scholar] [CrossRef]
  18. Martínez-Arias, C.; Witzell, J.; Solla, A.; Martin, J.A.; Rodríguez-Calcerrada, J. Beneficial and pathogenic plant-microbe interactions during flooding stress. Plant, Cell Environ. 2022, 45, 2875–2897. [Google Scholar] [CrossRef]
  19. Zhong, Y.; Guo, Z.; Wei, M.; Wang, J.; Song, S.; Chi, B.; Zhang, Y.; Liu, J.; Li, J.; Zhu, X.; et al. Hydrogen sulfide upregulates the alternative respiratory pathway in mangrove plant Avicennia marina to attenuate waterlogging-induced oxidative stress and mitochondrial damage in a calcium-dependent manner. Plant Cell Environ. 2023, 46, 1521–1539. [Google Scholar] [CrossRef]
  20. Pan, R.; Buitrago, S.; Feng, X.; Hu, A.; Zhou, M.; Zhang, W. Ethylene regulates aerenchyma formation in cotton under hypoxia stress by inducing the accumulation of reactive oxygen species. Environ. Exp. Bot. 2022, 197, 104826. [Google Scholar] [CrossRef]
  21. Tian, L.-X.; Zhang, Y.-C.; Chen, P.-L.; Zhang, F.-F.; Li, J.; Yan, F.; Dong, Y.; Feng, B.-L. How does the waterlogging regime affect crop yield? A global meta-analysis. Front. Plant Sci. 2021, 12, 634898. [Google Scholar] [CrossRef]
  22. Voesenek, L.A.C.J.; Bailey-Serres, J. Flood adaptive traits and processes: An overview. New Phytol. 2015, 206, 57–73. [Google Scholar] [CrossRef]
  23. Loreti, E.; van Veen, H.; Perata, P. Plant responses to flooding stress. Curr. Opin. Plant Biol. 2016, 33, 64–71. [Google Scholar] [CrossRef]
  24. Jia, W.; Ma, M.; Chen, J.; Wu, S. Plant morphological, physiological and anatomical adaption to flooding stress and the underlying molecular mechanisms. Int. J. Mol. Sci. 2021, 22, 1088. [Google Scholar] [CrossRef]
  25. Yin, C.; Huang, Y.; Zhang, X.; Zhou, Y.; Chen, S.; Zhang, J. Ethylene-mediated regulation of coleoptile elongation in rice seedlings. Plant Cell Environ. 2023, 46, 1060–1074. [Google Scholar] [CrossRef]
  26. Daniel, K.; Hartman, S. How plant roots respond to waterlogging. J. Exp. Bot. 2024, 75, 511–525. [Google Scholar] [CrossRef]
  27. Khan, M.I.R.; Trivellini, A.; Chhillar, H.; Chopra, P.; Ferrante, A.; Khan, N.A.; Ismail, A.M. The significance and functions of ethylene in flooding stress tolerance in plants. Environ. Exp. Bot. 2020, 179, 104188. [Google Scholar] [CrossRef]
  28. McGee, T.; Shahid, M.A.; Beckman, T.G.; Chaparro, J.X.; Schaffer, B.; Sarkhosh, A. Physiological and biochemical characterization of six Prunus rootstocks in response to flooding. Environ. Exp. Bot. 2021, 183, 104368. [Google Scholar] [CrossRef]
  29. Wu, W.; Zhou, R.-C.; Ni, G.-Y.; Shen, H.; Ge, X.-J. Is a new invasive herb emerging? Molecular confirmation and preliminary evaluation of natural hybridization between the invasive Sphagneticola trilobata (Asteraceae) and its native congener S. calendulacea in South China. Biol. Invasions 2013, 15, 75–88. [Google Scholar] [CrossRef]
  30. Li, H.M.; Ren, C.; Yang, Q.-E.; Yuan, Q. A new natural hybrid of Sphagneticola (Asteraceae, Heliantheae) from Guangdong, China. Phytotaxa 2015, 221, 71. [Google Scholar]
  31. Ni, G.Y.; Zhao, P.; Wu, W.; Lu, X.K.; Zhao, X.H.; Zhu, L.W.; Niu, J.F. A hybrid of the invasive plant has similar competitive ability but different response to nitrogen deposition compared to parent. Ecol. Res. 2014, 29, 331–339. [Google Scholar] [CrossRef]
  32. Gao, L.; Cai, M.; Zeng, L.; Zhang, Q.; Zhu, H.; Gu, X.; Peng, C. Adaptation of the invasive plant (Sphagneticola trilobata L. Pruski) to a high cadmium environment by hybridizing with native relatives. Front. Plant Sci. 2022, 13, 905577. [Google Scholar] [CrossRef]
  33. Zhang, Q.; Chen, G.; Shao, L.; Gu, X.; Huang, J.; Peng, C. The hybridization between Sphagneticola trilobata (L.) Pruski and Sphagneticola calendulacea (L.) Pruski improved the tolerance of hybrid to cadmium stress. Chemosphere 2020, 249, 126540. [Google Scholar] [CrossRef]
  34. Zhang, Q.L.; Chen, G.X.; Huang, J.D.; Peng, C.L. Comparison of the ability to control water loss in the detached leaves of Wedelia trilobata, Wedelia chinensis, and their hybrid. Plants 2020, 9, 1227. [Google Scholar] [CrossRef]
  35. Zhang, Q.L.; Huang, J.D.; Ke, W.Q.; Cai, M.L.; Chen, G.X.; Peng, C.L. Responses of Sphagneticola trilobata, Sphagneticola calendulacea and their hybrid to drought stress. Int. J. Mol. Sci. 2021, 22, 11288. [Google Scholar] [CrossRef]
  36. Culley, T.M.; Hardiman, N.A. The role of intraspecific hybridization in the evolution of invasiveness: A case study of the ornamental pear tree Pyrus calleryana. Biol. Invasions 2009, 11, 1107–1119. [Google Scholar] [CrossRef]
  37. Sun, Z.; Chen, Y.; Schaefer, V.; Liang, H.; Li, W.; Huang, S.; Peng, C. Responses of the hybrid between Sphagneticola trilobata and Sphagneticola calendulacea to low temperature and weak light characteristic in South China. Sci. Rep. 2015, 5, 16906. [Google Scholar] [CrossRef]
  38. Ding, Z.; Sun, Q. Effects of flooding depth on metal(loid) absorption and physiological characteristics of Phragmites australis in acid mine drainage phytoremediation. Environ. Technol. Innov. 2021, 22, 101512. [Google Scholar] [CrossRef]
  39. Mozo, I.; Rodríguez, M.E.; Monteoliva, S.; Luquez, V.M.C. Floodwater depth causes different physiological responses during post-flooding in Willows. Front. Plant Sci. 2021, 12, 575090. [Google Scholar] [CrossRef]
  40. Haque, A.; Rafii, M.Y.Y.; Yusoff, M.M.; Ali, N.S.; Yusuff, O.; Arolu, F.; Anisuzzaman, M. Flooding tolerance in Rice: Adaptive mechanism and marker-assisted selection breeding approaches. Mol. Biol. Rep. 2023, 50, 2795–2812. [Google Scholar] [CrossRef]
  41. Muhammad, T.; Zhang, J.; Ma, Y.; Li, Y.; Zhang, F.; Zhang, Y.; Liang, Y. Overexpression of a mitogen-activated protein kinase SlMAPK3 positively regulates tomato tolerance to cadmium and drought stress. Molecules 2019, 24, 556. [Google Scholar] [CrossRef]
  42. Mushtaq, N.; Wang, Y.; Fan, J.M.; Li, Y.; Ding, J. Down-regulation of Cytokinin receptor gene SlHK2 improves plant tolerance to drought, heat, and combined stresses in tomato. Plants 2022, 11, 154. [Google Scholar] [CrossRef]
  43. Mao, C.; Lu, S.; Lv, B.; Zhang, B.; Shen, J.; He, J.; Luo, L.; Xi, D.; Chen, X.; Ming, F. A rice NAC transcription factor promotes leaf senescence via ABA biosynthesis. Plant Physiol. 2017, 174, 1747–1763. [Google Scholar] [CrossRef]
  44. Nguyen, K.H.; Van Ha, C.; Nishiyama, R.; Watanabe, Y.; Leyva-González, M.A.; Fujita, Y.; Tran, U.T.; Li, W.Q.; Tanaka, M.; Seki, M.; et al. Arabidopsis type B cytokinin response regulators ARR1, ARR10, and ARR12 negatively regulate plant responses to drought. Proc. Natl. Acad. Sci. USA 2016, 113, 3090–3095. [Google Scholar] [CrossRef]
  45. Yamauchi, T.; Nakazono, M. Mechanisms of lysigenous aerenchyma formation under abiotic stress. Trends Plant Sci. 2022, 27, 13–15. [Google Scholar] [CrossRef]
  46. Yeung, E.; van Veen, H.; Vashisht, D.; Paiva, A.L.S.; Hummel, M.; Rankenberg, T.; Steffens, B.; Steffen-Heins, A.; Sauter, M.; de Vries, M.; et al. A stress recovery signaling network for enhanced flooding tolerance inArabidopsis thaliana. Proc. Natl. Acad. Sci. USA 2018, 115, E6085–E6094. [Google Scholar] [CrossRef]
  47. Xu, H.; Wang, S.; Larkin, R.M.; Zhang, F. The transcription factors DcHB30 and DcWRKY75 antagonistically regulate ethylene-induced petal senescence in carnation (Dianthus caryophyllus). J. Exp. Bot. 2022, 73, 7326–7343. [Google Scholar] [CrossRef]
  48. Zhang, H.M.; Li, S.; Yang, L.; Cai, G.H.; Chen, H.M.; Gao, D.L.; Lin, T.; Cui, Q.Z.; Wang, D.H.; Li, Z.; et al. Gain-of-function of the 1-aminocyclopropane-1-carboxylate synthase gene induces female flower development in cucumber gynoecy. Plant Cell 2021, 33, 306–321. [Google Scholar] [CrossRef]
  49. Zhang, Q.; Zhai, J.; Shao, L.; Lin, W.; Peng, C. Accumulation of anthocyanins: An adaptation strategy of Mikania micrantha to low temperature in winter. Front. Plant Sci. 2019, 10, 1049. [Google Scholar] [CrossRef]
  50. Baker, N.R. Chlorophyll fluorescence: A probe of photosynthesis in vivo. Annu. Rev. Plant Biol. 2008, 59, 89–113. [Google Scholar] [CrossRef]
  51. Krall, J.P.; Edwards, G.E. Relationship between photosystem II activity and CO2 fixation in leaves. Physiol. Plantarum 1992, 86, 180–187. [Google Scholar] [CrossRef]
  52. Oxborough, K.; Baker, N.R. Resolving chlorophyll a fluorescence images of photosynthetic efficiency into photochemical and non-photochemical components—Calculation of qP and Fv’/Fm’; without measuring Fo’. Photosynth. Res. 1997, 54, 135–142. [Google Scholar] [CrossRef]
  53. Lee, S.-H.; Sakuraba, Y.; Lee, T.; Kim, K.-W.; An, G.; Lee, H.Y.; Paek, N.-C. Mutation of Oryza sativa CORONATINE INSENSITIVE 1b (OsCOI1b) delays leaf senescence. J. Integr. Plant Biol. 2015, 57, 562–576. [Google Scholar] [CrossRef]
  54. Liu, Y.; Ren, D.; Pike, S.; Pallardy, S.; Gassmann, W.; Zhang, S. Chloroplast-generated reactive oxygen species are involved in hypersensitive response-like cell death mediated by a mitogen-activated protein kinase cascade. Plant J. 2007, 51, 941–954. [Google Scholar] [CrossRef]
  55. Lim, T.S.; Chitra, T.R.; Han, P.; Pua, E.C.; Yu, H. Cloning and characterization of and flavin-containing amine oxidases. J. Exp. Bot. 2006, 57, 4155–4169. [Google Scholar] [CrossRef]
  56. Livak, K.J.; Schmittgen, T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 2001, 25, 402–408. [Google Scholar] [CrossRef]
  57. Gallego-Tévar, B.; Grewell, B.J.; Futrell, C.J.; Drenovsky, R.E.; Castillo, J.M. Interactive effects of salinity and inundation on native Spartina foliosa, invasive S. densiflora and their hybrid from San Francisco Estuary, California. Ann. Bot. 2020, 125, 377–389. [Google Scholar] [CrossRef]
Ijms 25 06738 g001
Figure 1. Phenotypic changes in the hybrid species Sphagneticola × guangdongensis, invasive species S. trilobata, and native species S. calendulacea at 0, 6, 9, and 12 days under flooding stress (a–d); the phenotypic changes in Sphagneticola × guangdongensis and its parents after 2 days of flooding stress (e–g).
Figure 1. Phenotypic changes in the hybrid species Sphagneticola × guangdongensis, invasive species S. trilobata, and native species S. calendulacea at 0, 6, 9, and 12 days under flooding stress (a–d); the phenotypic changes in Sphagneticola × guangdongensis and its parents after 2 days of flooding stress (e–g).
Ijms 25 06738 g001
Ijms 25 06738 g002
Figure 2. Tissue localization of hydrogen peroxide (a,b) and superoxide anions (c,d); changes in malondialdehyde (MDA, e) content, electrolytic leakage (f), Rubisco large subunit (RubL, k), and increased dry weight (l) under flooding stress for 12 days, compared with the control. Changes in the maximum photochemical efficiency (Fv/Fm, g), photosynthetic electron transport rate (ETR, h), net photosynthetic rate (Pn, i), and content of chlorophyll (j) under flooding stress. There were five biological replicates. Different letters (a, b, c, d) above bars indicate significant differences (p < 0.05).
Figure 2. Tissue localization of hydrogen peroxide (a,b) and superoxide anions (c,d); changes in malondialdehyde (MDA, e) content, electrolytic leakage (f), Rubisco large subunit (RubL, k), and increased dry weight (l) under flooding stress for 12 days, compared with the control. Changes in the maximum photochemical efficiency (Fv/Fm, g), photosynthetic electron transport rate (ETR, h), net photosynthetic rate (Pn, i), and content of chlorophyll (j) under flooding stress. There were five biological replicates. Different letters (a, b, c, d) above bars indicate significant differences (p < 0.05).
Ijms 25 06738 g002
Ijms 25 06738 g003
Figure 3. Adventitious roots under flooding stress for 5 and 24 h (a). The occurrence rate of adventitious roots under flooding stress (c). The biological replicates were forty. Aerenchyma (b), number of stem nodes (d), and length of stem nodes (e) under flooding stress for 12 days, compared with the control. There were ten biological replicates. Different letters (a, b, c, d) above bars indicate significant differences (p < 0.05).
Figure 3. Adventitious roots under flooding stress for 5 and 24 h (a). The occurrence rate of adventitious roots under flooding stress (c). The biological replicates were forty. Aerenchyma (b), number of stem nodes (d), and length of stem nodes (e) under flooding stress for 12 days, compared with the control. There were ten biological replicates. Different letters (a, b, c, d) above bars indicate significant differences (p < 0.05).
Ijms 25 06738 g003
Ijms 25 06738 g004
Figure 4. Percentage increase in ethylene content under flooding stress (a). Heat map of the genes related to ethylene synthesis and transduction (b) and expression of the selected genes were validated by real-time PCR under flooding stress and in the control group (c–f). There were three biological replicates. Different letters (a, b, c) above bars indicate significant differences (p < 0.05).
Figure 4. Percentage increase in ethylene content under flooding stress (a). Heat map of the genes related to ethylene synthesis and transduction (b) and expression of the selected genes were validated by real-time PCR under flooding stress and in the control group (c–f). There were three biological replicates. Different letters (a, b, c) above bars indicate significant differences (p < 0.05).
Ijms 25 06738 g004
Ijms 25 06738 g005
Figure 5. Schematic diagram of adaptation strategies to flooding stress in Sphagneticola × guangdongensis and its parents. Under flooding stress, the invasive species S. trilobata could not effectively synthesize and accumulate ethylene, resulting in a small number of adventitious roots and aerenchyma. However, the hybrid species Sphagneticola × guangdongensis and native species S. calendulacea synthesized and accumulated a large amount of ethylene rapidly, promoting the generation of adventitious roots and aerenchyma, which resulted in the resistance of Sphagneticola × guangdongensis and the native species being stronger than that of the invasive species.
Figure 5. Schematic diagram of adaptation strategies to flooding stress in Sphagneticola × guangdongensis and its parents. Under flooding stress, the invasive species S. trilobata could not effectively synthesize and accumulate ethylene, resulting in a small number of adventitious roots and aerenchyma. However, the hybrid species Sphagneticola × guangdongensis and native species S. calendulacea synthesized and accumulated a large amount of ethylene rapidly, promoting the generation of adventitious roots and aerenchyma, which resulted in the resistance of Sphagneticola × guangdongensis and the native species being stronger than that of the invasive species.
Ijms 25 06738 g005
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.

Share and Cite

MDPI and ACS Style

Zhang, Q.; Chen, G.; Ke, W.; Peng, C. Adaptation of the Invasive Plant Sphagneticola trilobata to Flooding Stress by Hybridization with Native Relatives. Int. J. Mol. Sci. 2024, 25, 6738. https://doi.org/10.3390/ijms25126738

AMA Style

Zhang Q, Chen G, Ke W, Peng C. Adaptation of the Invasive Plant Sphagneticola trilobata to Flooding Stress by Hybridization with Native Relatives. International Journal of Molecular Sciences. 2024; 25(12):6738. https://doi.org/10.3390/ijms25126738

Chicago/Turabian Style

Zhang, Qilei, Guangxin Chen, Weiqian Ke, and Changlian Peng. 2024. "Adaptation of the Invasive Plant Sphagneticola trilobata to Flooding Stress by Hybridization with Native Relatives" International Journal of Molecular Sciences 25, no. 12: 6738. https://doi.org/10.3390/ijms25126738

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop