Effects of soil drought on competitiveness of the invasive weed Aegilops tauschii

doi:10.21203/rs.3.rs-4311260/v1

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Effects of soil drought on competitiveness of the invasive weed Aegilops tauschii

https://doi.org/10.21203/rs.3.rs-4311260/v1

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Aegilops tauschii, an invasive weed, has a detrimental impact on the winter wheat cultivation areas of China. Understanding how drought influences competitive ability of A. tauschii can help identify traits related to its invasiveness and guide management. Slight, moderate, and severe soil drought stress conditions were established using potted weighing and water control methods. Concurrently, the de Wit replacement experiment was conducted to assess changes in morphological structure, biomass allocation, and physiological characteristics under varying intensities of soil drought stress. Based on observations of alterations in plant height, total leaf area, and total biomass, two-factor variance analysis revealed that soil drought inhibited the growth and development of both A. tauschii and Triticum aestivum L. (‘Xinmai 32’). Furthermore, one-factor variance analysis revealed that A. tauschii and wheat responded to soil drought stress by increasing superoxide dismutase (SOD) activity and proline content. However, as drought severity escalated, chlorophyll content in A. tauschii and wheat declined significantly, while relative electrical conductivity (REC) and thiobarbituric acid (TBA) content increased markedly. The results of the fuzzy membership function indicated that A. tauschii exhibited greater drought tolerance compared to the tested wheat variety. Lastly, considering adjustments in the corrected index of relative competition intensity (CRCI), it was observed that soil drought amplified the competitive inhibition of A. tauschii on wheat. In short, A. tauschii was more tolerant of the soil drought stress than wheat through the favorable adjustment of morphology, biomass allocation pattern and physiological features, and soil drought intensified its competitive inhibition on wheat.

soil drought

Aegilops tauschii

competitiveness

protective enzyme activity

wheat

Soil water is an important factor that limits plant growth, development, and distribution. Extreme weather, including drought, may affect the colonization and competition of alien plants to promote their invasion (O’Briain 2019; Diez et al. 2012). Some studies have shown that invasive plants may outcompete native species in dry conditions (Paudel et al. 2018), even if the native species are adapted to the arid environment (Mason et al. 2012). Invasive plants may benefit from soil drought due to their broader environmental tolerance and greater phenotypic plasticity compared to native species (Santamarina et al. 2022). Soil drought may increase the competitiveness of invasive plant species through changes in allelopathy or by changing the functional differences between invasive and native species (Lu et al. 2022; Wang et al. 2020a; Yu et al. 2022). However, some studies have also reported that soil drought has a greater negative effect on invasive plants than on native species (Liu et al. 2017; Valliere et al. 2019). The competitive interaction between invasive plants and native species and their relationship with resource gradients have gained much attention (Leal et al. 2022). Competition is a key factor affecting community composition and plant invasion (Kuebbing and Nuñez 2016). Therefore, information on the competitiveness of invasive plants under different soil drought conditions is necessary, as it can act as a reference for early warning of their spread.

Aegilops tauschii is one of the 10 most noxious weeds in the world. Wild populations of A. tauschii can be found in the arid and semi-arid regions of Central Eurasia (Van Slageren 1994). With a wide range of adaptations, the species is invasive in wheat fields and distributed from arid deserts to humid temperate forests (Fang 2012). Ever since Ye Dexian collected the first specimen of A. tauschii in Xinxiang, Henan (China) in 1955, it has invaded and spread to many major wheat-producing provinces in China, such as Shaanxi, Shanxi, Shandong, and Anhui (Wang and Chen 2019). As the progenitor of the D subgenome of wheat, A. tauschii shares some biological and genetic characteristics with wheat, which increases the difficulty of developing selective herbicides to control it (Yu and Li 2018). A. tauschii not only competes with wheat for water, fertilizer, and other resources but also acts as an alternative host for wheat stripe rust, which can easily lead to a reduction in wheat yield or total failure of wheat. The areas affected by A. tauschii have increased, and it has become one of the most hazardous gramineous weeds in winter wheat growing areas in China (Qiang and Zhang 2022). Previous studies by our research group have shown that A. tauschii is drought-resistant, as determined by changes in biomass allocation patterns and allelochemical inputs (Wang et al. 2018), as well as plastic changes in morphological and physiological characteristics (Wang et al. 2019a). However, there are no reports on the effect of soil drought on its competitiveness. Therefore, in this study, we addressed the following questions: (1) Does soil drought affect the competition between A. tauschii and wheat? (2) Does soil drought affect the invasion and spread of A. tauschii in arid areas?

Seed collection

In June 2022, the tested A. tauschii and wheat (Triticum aestivum L. ‘Xinmai 32’) seeds were obtained from the experimental field (35°18’ N, 113°52’ E) of Xinxiang Academy of Agricultural Sciences in Henan Province of China, and they were dried and stored indoors. The experiment was conducted in the Science and Education Experimental Park of Henan University of Science and Technology. The study area is located in Luolong District, Luoyang City, Henan Province (34°59’ N, 112°16’ E). It has a temperate monsoon climate, with an average annual temperature of 14.86°C and an average annual precipitation of 578.2 mm.

Experimental design

In September 2022, the screened A. tauschii and wheat seeds were sown on the surface of planting box (60 cm x 40 cm x 20 cm) and covered with 1 to 2 cm thick matrix (i.e. perlite, vermiculite, and peat mixed in a 1:1:1 ratio). Germination was accelerated in an illuminated incubator (day/night: 25°C/20°C, 12 h each). After the seeds germinated, the planting box was moved outdoors for normal management. When growing to the period of "two complete leaves and one young leaf" (i.e., the early stage of tillering) (Hyles et al. 2020), A. tauschii and wheat seedlings of a similar height and growth vigor were selected and transplanted into pots with a diameter of 21 cm at the opening and a height of 19 cm, according to the requirements of the experimental design. The potting soil was dried to constant weight in an oven at 105°C in advance, and the dried soil was 5 kg·pot^–1. Four intensities of drought stress were used: normal level (NL) (75–80% of the maximum water holding capacity in the field), light drought (LD) (60–70% of the maximum water holding capacity in the field), moderate drought (MD) (55–60% of the maximum water holding capacity in the field), and severe drought (SD) (45–50% of the maximum water holding capacity in the field) (Huang et al. 2013; Wang et al. 2019a).

Considering the common planting density of wheat (300 plants·m^–2), the pot specifications, and the edge effect, the planting density was set to 12 plants·pot^–1. According to the de Wit (1960) replacement experiment, A. tauschii and wheat were planted separately and together in an equal proportion, with the same planting density in each pot. After slow growth for one week, the seedlings were managed normally, and soil water was controlled when the seedlings grew to the period of “three complete leaves and one young leaf”. Under drought stress, the soil water content (SWC) was controlled using the weighing method; the SWC was weighed every two days. When the SWC was lower than the set range, water was added slowly to replenish soil water. Five pots were treated each, with 60 pots in total. Each pot was placed on a tray while watering, and the overflowing water was poured back into the pot. To prevent rainfall from interfering with soil water, the experiment was conducted in a rain shelter. After 60 days of incubation, the experiment was concluded, and relevant indices such as morphology, biomass, and physiological properties were measured.

Morphological and biomass-related indices

In single-planting and mixed-planting modes, five pots were selected for each treatment, and three plants were selected from the same position of each pot. After measuring the height of each plant, the roots of the plants were carefully separated from the soil by water flushing to minimize the loss of fine roots. Next, the leaf area was measured with a scanner and Adobe Photoshop 2020 as in (Xiao et al, 2005). Finally, the roots, stems, and leaves of the plants were separated, placed in paper bags, dried to a constant weight in an oven at 80°C, and then weighed using a 1/10,000 balance. The root-shoot ratio (RSR) was determined as follows: RSR = root biomass/aboveground biomass.

Physiological indices

Three pots of the single-planted A. tauschii and wheat were selected for each treatment, and three plants were randomly selected from each pot. An appropriate number of mature leaves (the third or fourth leaf from top to bottom) were cut (about 2.00 g fresh weight per treatment) to measure the following physiological indicators. The chlorophyll (a + b) content of the plants was determined using the 95% ethanol method (Li 2000; Zou 2003); The nitro blue tetrazolium (NBT) photoreduction method was used to measure the SOD content; the thiobarbituric acid reactive substance (TBARS) assay was performed to measure the TBA content; and the acidic ninhydrin assay was performed to measure the proline content (Li 2000; Zou 2003). The relative electric conductivity (REC) was determined as described by Zou (2003) with slight improvement.

Data analysis

The relative neighbor effect (RNE) and corrected index of relative competition intensity (CRCI) were used to determine the competition between A. tauschii and wheat (Oksanen et al. 2006; Manea and Leishman 2011).

RNE = (X-Y)/max(X,Y)

CRCI = arcsin (RNE)

Here, X indicates the total biomass (dry weight) of the single-planted A. tauschii, and Y indicates the total biomass of the mixed-planted A. tauschii. CRCI = 0 indicates that A. tauschii has no competitive effect on wheat; CRCI > 0 indicates that A. tauschii weakened the growth of wheat; CRCI < 0 indicates that A. tauschii promotes the growth of wheat.

The membership function was used to comprehensively evaluate the drought resistance of A. tauschii and wheat (Wang et al. 2023a) using the following equation:

Z _ij = (X_ij-X_ijmin)/(X_ijmax-X_ijmin)

Here, Z_ij indicates the measured value of index j of plant i, X_min indicates the minimum value of the measured index, and X_max indicates the maximum value of the measured index. SOD, proline, and chlorophyll contents were positively correlated with drought resistance, and their membership function values were Z_ij; REC and TBARS content were negatively correlated with drought resistance, and their membership function values were 1-Z_ij. The mean of the sum of the membership function values of all indices was calculated, and the mean value was positively correlated with drought tolerance.

SPSS18.0 and Microsoft Excel were used for data analysis and graphing. All data were evaluated by one- and two-way analysis of variance (ANOVA). Means were compared by Duncan’s post hoc test at p < 0.05. Two-factor variance was used to analyze the effects of soil drought and planting mode on the morphology and biomass of A. tauschii and wheat. One-factor variance was used to analyze the effects of soil drought on the physiology, biochemistry, and competitiveness of A. tauschii and wheat.

The results of the two-factor variance analysis showed that soil drought stress significantly affected the plant height, total leaf area, total biomass, and RSR of A. tauschii and wheat (Table 1, Figs. 1, 2 and 3). The planting mode did not significantly affect the above indices of the two species (Table 1, Figs. 1, 2 and 3). The interaction between soil drought stress and planting mode significantly affected only the plant height and total biomass of wheat, but it did not significantly affect other morphological and biomass indicators of A. tauschii and wheat (Table 1).

Table 1

The results of the analysis of variance (p values) of growth indicators and the competition index of *A. tauschii* with different soil drought stress and planting patterns
Parameter	A. tauschii				T. aestivum
Parameter	Soil drought	Planting pattern	Soil drought × planting pattern	Soil drought	Planting pattern	Soil drought × planting pattern
Plant height	<0.01	0.11	0.37	<0.01	0.06	<0.01
Total leaf area	<0.01	0.09	0.23	<0.01	0.14	0.69
Total biomass	<0.01	0.05	0.19	<0.01	0.15	<0.01
RSR	<0.01	0.06	0.16	<0.01	0.05	0.89

The plant height and total leaf area of single-planted and mixed-planted A. tauschii and wheat decreased as the intensity of soil drought increased (Fig. 1). The plant height of mixed-planted A. tauschii was significantly different between the NL and SD groups (P < 0.05), whereas the difference in the plant height of single-planted A. tauschii was not significant. For the mixed-planted wheat, their heights were significantly different already between the MD and NL groups (P < 0.05), while for the singled-planted wheat, their plant heights were significantly different only between the SD and NL groups (P < 0.05). The plant heights of single-planted and mixed-planted A. tauschii decreased by 18.64% and 27.22%, respectively, and those of single-planted and mixed-planted wheat decreased by 26.86% and 34.05%, respectively, in the SD group compared to the height of the respective plants in the NL group. No significant difference was found in the total leaf area of single-planted A. tauschii between the NL and SD groups. In contrast, the total leaf areas of mixed-planted A. tauschii, single-planted wheat, and mixed-planted wheat in the SD group were significantly different from those in their respective NL groups (P < 0.05). Compared to the NL group, in the SD group, the total leaf area values of single-planted and mixed-planted A. tauschii decreased by 19.29% and 32.68%, respectively; the decrease in height was 39.01% and 43.45% in wheat.

The total biomass of single-planted and mixed-planted A. tauschii and wheat decreased with a decrease in soil water (Fig. 2). The total biomass of the single-planted A. tauschii in the SD group was not significantly different from that in the NL group, whereas the total biomass of the mixed-planted A. tauschii, of singled-planted and of mixed-planted wheat were significantly different between the SD and NL groups (P < 0.05). Compared to the NL group, in the SD group, the total biomass of single-planted and mixed-planted A. tauschii decreased by 26.92% and 35.89%, respectively; whilst the decrease in total biomass was 47.36% and 56.46% in wheat.

The RSR of A. tauschii and wheat, single-planted and mixed-planted, increased as soil water decreased (Fig. 3). The RSR of A. tauschii in both planting modes differed significantly between the NL and SD groups (P < 0.05), whereas the RSR of wheat in the two planting modes showed no significant difference. Compared to the NL group, in the SD group, the RSR of single-planted and mixed-planted A. tauschii increased by 39.22% and 28.00%, respectively; the increase in the RSR of wheat was 29.09% and 27.78%, respectively.

The REC and proline content of single-planted A. tauschii and wheat increased as the intensity of soil drought increased (Fig. 4). The REC of A. tauschii and wheat in the SD groups were significantly different (P < 0.05) from that in the NL group. The REC of A. tauschii in the SD group increased by 42.86% compared to that in the NL group, which was less than the increase in REC recorded for wheat (75.02%). The proline content of A. tauschii and wheat increased significantly (P < 0.05; by 53.46% and 85.16%, respectively) in the SD group, compared to that in the NL group.

As the soil was further dried, higher SOD activity and TBARS contents were recorded in single-planted A. tauschii and wheat (Fig. 5). The SOD activity of both species in the LD group was significantly different from that in the NL group (P < 0.05). The SOD activity of A. tauschii and wheat in the SD group increased by 63.98% and 60.99%, respectively, compared to that in the respective NL group. However, the SOD activity of wheat was not significantly different between the SD and MD groups. The TBARS content of A. tauschii and wheat in the MD and LD groups was significantly different (P < 0.05) from that in the NL group. The TBARS content of A. tauschii and wheat in the SD group increased by 74.05% and 92.26%, respectively, compared to that in the NL group.

The chlorophyll content of A. tauschii and wheat decreased as the intensity of soil drought increased (Fig. 6); the chlorophyll content decreased significantly (P < 0.05) in the SD and in wheat also in the MD groups, respectively, compared to that in the NL group. The chlorophyll content of A. tauschii and wheat in the SD group decreased by 53.46% and 85.16%, respectively, compared to that in the plants in the NL group.

The membership function values of the five indices (REC, proline content, SOD activity, TBARS content, and chlorophyll content) calculated by the membership function method are presented in Table 2. The rankings of the mean value suggested that A. tauschii had a higher drought tolerance than the tested wheat variety (‘Xinmai 32’).

Table 2

Comprehensive evaluation of drought resistance in *A. tauschii* and *T. aestivum*
Species	Membership function value					Average value	Order
Species	Relative conductivity	Proline content	SOD activity	TBARS content	Chlorophyll content	Average value	Order
A. tauschii	0.3985	0.6381	0.4933	0.3847	0.5412	0.4912	1
T. aestivum	0.6143	0.2127	0.6364	0.3434	0.4136	0.4441	2

The results showed that CRCI of A. tauschii increased as soil drought intensified (Fig. 7), and a significant difference in CRCI (P < 0.05) was recorded between the SD and NL groups, while the difference was not significant between the SD and MD groups.

Plant height and leaf size affect the ability of plants to compete for sunlight, and therefore, they are widely used to assess plant responses to environmental changes (Gorchov and Trisel 2003; Wang et al. 2022). Biomass reduction caused by drought stress is one of the main effects on plants (Farrukh et al. 2023). Studies have shown that drought stress decreases plant height (Chadha et al. 2019; Abbas et al. 2022), leaf area (Momayyezi and Upadhyaya 2017) and total biomass (Zhao et al. 2021) of invasive plants. In this study, the plant height, total leaf area, and total biomass of single-planted and mixed-planted A. tauschii and wheat decreased as the soil drought intensified. According to the results of the two-factor variance analysis, soil drought stress significantly inhibited the growth of both seedlings. Additionally, plant height, total leaf area, and total biomass of A. tauschii in the SD group (single-planted or mixed-planted) decreased less compared to those in the NL group than that of wheat, indicating that the inhibitory effect of drought stress on the growth of wheat seedlings was greater than that on the seedlings of A. tauschii. Additionally, the plant height, leaf area, and total biomass of mixed-planted A. tauschii and wheat were smaller than those of their single-planted species, probably because of interspecific competition or, more specifically, due to limited resources and space for growth under mixed cropping conditions. These findings were similar to those of studies on the invasive plant Amaranthus spinosus competing with A. tricolor (Wang et al. 2020a, 2020b; Wu et al. 2019; Yu et al. 2022).

Besides showing morphological differences, plants respond to environmental changes with different biomass allocation strategies (Chapin 1980; Aerts and Chapin 2000). The RSR is one of the commonly used indicators of the biomass allocation strategies of plants under stress (Shipley and Meziane 2002). According to the optimal allocation theory, when soil water is limited, plants allocate more photosynthetic products to their underground parts to maintain water absorption, thus increasing RSR (Xu et al. 2022; Wang and Taub 2010; Zheng et al. 2016).

In this study, the RSR of single-planted and mixed-planted A. tauschii and wheat increased continuously as soil drought intensified. This suggests that both species absorbed more water and decreased water loss by allocating more underground biomass and reducing aboveground biomass. This finding was similar to those reported in studies on the invasive plant species Cortaderia selloana (Domenech and Vila 2008). The increase in RSR of A. tauschii was higher than the increase in RSR of wheat. This finding indicated that compared to wheat, A. tauschii can allocate more biomass to its underground part to cope with soil drought stress.

The physiological response of plants plays an essential role in coping with abiotic stress (Khan et al. 2020). Chlorophyll content can be used as an indicator of the sensitivity of plants to drought stress (Wang et al. 2019b; Gholinezhad and Darvishzadeh, 2021). Studies have shown that drought stress inhibits chlorophyll biosynthesis and promotes chlorophyllase activity and its degradation rate, thus decreasing the chlorophyll content (Le Lay et al. 2001; Piveta et al. 2020). Other studies have reported the opposite pattern, i.e. that drought stress enhances the chlorophyll content, probably due to a decrease in water content during the stress period (Liang et al. 2009). Our results showed that as drought stress intensified, the chlorophyll content of A. tauschii and wheat seedlings decreased similarly to the findings of other studies (Wang et al. 2019a).

The REC indicates plant cell membrane permeability, whereas the TBARS content indicates membrane lipid peroxidation (Nischal and Dev Sharma 2020). Therefore, the REC and TBARS contents are key indicators of the plant plasma membrane damage due to abiotic stress. In this study, the REC and TBARS contents of A. tauschii and wheat increased as soil water content decreased, suggesting progressively intensifying damage to their plasma membranes caused by drought stress. As soil drought conditions changed from NL to SD, the increase in REC and the TBARS content of wheat was significantly higher than that of A. tauschii, indicating that the plasma membrane of A. tauschii was less affected than that of wheat under the same drought condition.

SOD is an important reactive oxygen-free radical scavenging enzyme in plants. Stress tolerance and SOD activity are generally found to be positively correlated (Wang et al. 2019a). Some studies have found that plants can prevent the overaccumulation of TBARS by scavenging excess reactive oxygen free radicals due to an increase in the activity of protective enzymes such as SOD, which prevents membrane lipid peroxidation and cell damage (Wang et al. 2019a). In this study, A. tauschii and wheat were found to cope with soil drought stress by increasing their SOD activity, similarly to the findings of a study on the invasive plant Rorippa amphibia (Zhou et al. 2022). The increase in the SOD activity of wheat was not significant as the condition changed from MD to SD, which might be related to the drought tolerance of this wheat variety.

Plant drought tolerance is a complex physiological process involving multiple factors. It can be comprehensively evaluated using membership function analysis, which adopts multi-index measurements to avoid single-index bias. This method is widely used in research on invasive plants, such as Ageratina adenophora (Su et al. 2005) and Avena sativa (Lin et al. 2021). In this study, five highly correlated indices, including SOD, TBARS, and REC, were calculated using the membership function method. The results showed that A. tauschii outperformed the tested wheat variety in terms of drought tolerance.

As biomass is an important measure of interspecific competition, changes in the biomass of mixed-planted plants are calculated and adopted by most competition indices to reflect interspecific competition (Freckleton and Watkinson 2000). In this study, the CRCI value of A. tauschii under drought stress was always greater than 0. It increased as drought severity intensified, indicating that A. tauschii outcompeted wheat under drought stress. The competitive advantage of A. tauschii might increase under drought stress due to its high relative competition intensity; similarly to data of a study on the invasive plant species Amaranthus spinosus (Yu et al. 2022). According to the stress gradient hypothesis (SGH), the net result of interspecies interactions in plants is the sum of facilitative and competitive interactions. As abiotic stress increases, promotion generally increases (Bertness and Callaway 1994), and this hypothesis is also supported by many studies (Callaway et al. 2002; Maestre et al. 2003; Liancourt et al. 2005). Changes in the CRCI value showed that the competitive inhibition of A. tauschii on wheat decreased in moderate-to-high drought stress treatments, which was in accordance with the SGH. Leal et al. (2022) studied the invasive plant Urochloa arrecta and also suggested that the success of invasive grass plants occurs due to their drought resistance rather than their high competitiveness. However, according to the findings in this study, regarding the effects of flooding (Wang et al. 2021), shading (Wang et al. 2022), and salt-alkali stress (Wang and Chen 2023) on the competitiveness of A. tauschii and its soil feedback, the successful invasion of A. tauschii is not only related to its outstanding adaptability but also may be related to its high competitiveness.

To summarize, A. tauschii exhibits high drought tolerance by adjusting its morphological structure, biomass allocation, and physiological characteristics. These changes increase its ability to cope with soil drought stress, and this might be a reason why it could outcompete the tested wheat variety under drought conditions. As A. tauschii is difficult to control, this species will further spread in China, especially in arid western areas.

Author contributions

Ning Wang: Data curation; methodology; formal analysis; writing; Hao Chen: Methodology; writing-review and editing; data curation; Lei Wang: Formal analysis; writing-review and editing; investigation.

Disclosure statement

No potential conflict of interest was reported by the authors.

Funding

This work was supported by the Natural Science Foundation of China (32271848) and the Natural Science Foundation of Henan Province (182300410092) and Public Welfare Industry Special Research Projects of Luoyang (2022087).

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30 Apr, 2024
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29 Apr, 2024
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Effects of soil drought on competitiveness of the invasive weed Aegilops tauschii

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Abstract

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Introduction

Material and methods

Seed collection

Experimental design

Morphological and biomass-related indices

Physiological indices

Data analysis

Results

Discussion

Conclusion

Declarations

References

Status:

Version 1