Next Article in Journal
Research on Recognition of Green Sichuan Pepper Clusters and Cutting-Point Localization in Complex Environments
Previous Article in Journal
Artificial Intelligence Models for Bankruptcy Prediction in Agriculture: Comparing the Performance of Artificial Neural Networks and Decision Trees
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Agriculture
Volume 15
Issue 10
10.3390/agriculture15101078
agriculture-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
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Article

Germination Under Temperature Stress Facilitates Invasion in Indehiscent Lepidium Species

by
Said Mohammed
1,2,*,† and
Klaus Mummenhoff
2
1
Department of Biology, College of Natural and Computational Sciences, Debre Berhan University, Debre Berhan P.O. Box 445, Ethiopia
2
Department of Biology, University of Osnabrück, Barbarastraße 11, D-49076 Osnabrück, Germany
*
Author to whom correspondence should be addressed.
†
Current address: Plant Ecology Group, Institute of Evolution and Ecology, University of Tübingen, Auf der Morgenstelle 5, D-72076 Tübingen, Germany.
Agriculture 2025, 15(10), 1078; https://doi.org/10.3390/agriculture15101078
Submission received: 18 February 2025 / Revised: 28 April 2025 / Accepted: 15 May 2025 / Published: 16 May 2025
(This article belongs to the Section Seed Science and Technology)
Browse Figures
Versions Notes

Abstract

:
This study investigates the germination ecology of three Lepidium species, including the invasive, indehiscent-fruited Lepidium appelianum and Lepidium draba, and the invasive, dehiscent-fruited Lepidium campestre. The ability of Lepidium species to germinate under a wide range of temperature conditions is significant for understanding their potential invasiveness and establishment in novel and extreme environments. This study aims to clarify the germination behavior of L. appelianum, L. draba, and L. campestre, thereby enhancing our understanding of their invasive potential and ecological implications in the context of a changing climate. The base (Tb), optimum (To), and maximum temperatures for 50% germination (Tc(50)) were determined across a broad thermal gradient following standard protocols. Freshly harvested seeds and fruits of L. appelianum are non-dormant. In contrast, L. draba exhibit pericarp-mediated chemical dormancy, while L. campestre demonstrates physiological dormancy, which is released through after-ripening. The results indicate that L. appelianum and L. draba seeds and fruits germinate at a base temperature (Tb) of 1 °C and 4 °C, respectively. On the other hand, L. campestre seeds germinate at a Tb of 5.8 °C. The optimum temperature (To) for the germination of seeds and fruits in L. appelianum and L. draba ranges from 23 °C to 25 °C, while the To for L. campestre seed germination is 16 °C to 18 °C. Additionally, the maximum temperature for 50% germination (Tc(50)) for L. appelianum fruits is 39.8 °C, for L. draba it is 34.4 °C, and L. campestre reports a (Tc(50)) ranging from 27.4 °C to 33.3 °C for freshly harvested and after-ripened seeds, respectively. These results demonstrated that L. appelianum and L. draba can germinate across a broad temperature range, from very cold to very hot, unlike L. campestre. These findings suggest that the unique reproductive strategy of indehiscent fruits, coupled with a wide thermal germination niche, may contribute to the invasive success of L. appelianum and L. draba. Given the projected climate warming, the results highlight the potential for increased invasiveness of these species and suggest the need for targeted management strategies.

1. Introduction

The germination stage plays a critical role in the life cycle of invasive plants, as successful germination is vital for the establishment of new populations [1,2]. The timing of emergence determines the initial environmental conditions experienced by seedlings, and therefore, the abiotic signals that trigger germination significantly impact plant survival and establishment [3,4]. Notably, temperature is the most influential factor in regulating germination and it serves a crucial role in determining seed germination [5,6]. The speed and germination percentage of seeds are directly impacted by temperature, as it affects water absorption and various physiological and biochemical reactions necessary for germination to occur [7,8,9]. Different plant species exhibit varying temperature requirements for germination, with some species capable of germinating across a wide range of temperatures, while others have more specific temperature preferences [1,10,11].
The capacity to germinate under diverse conditions may contribute to invasiveness by expanding potential suitable habitats and increasing the likelihood of establishment in new environments [12]. Given that plants may encounter varied environmental conditions after dispersal to new locations, broad temperature requirements for germination may significantly show species invasiveness [5,6]. Within our study systems, we focus on the closely related invasive species Lepidium appelianum and L. draba, which produce indehiscent fruits, as well as Lepidium campestre, which produces dehiscent fruits (Figure 1). L. appelianum Al-Shehbaz (syn. Cardaria pubescens (C. A. Meyer) Jarmolenko, Hymenophysa pubescens C. A. Meyer) is commonly referred to as globe-podded hoary cress, and L. draba L. (syn. Cardaria draba (L.) Desvaux) is known as heart-podded hoary cress [13,14,15]; Figure 1. On the other hand, the dehiscent fruit-producing L. campestre (L.) (Linnaeus) W. T. Aiton is commonly known as field pepperwort [16]; Figure 1. L. appelianum is native to Central Asia, including Kazakhstan and Uzbekistan, where it experiences a harsh continental climate with hot, dry summers and cold winters [17,18]. This invasive weed has also spread to Argentina, Australia, Canada, and the USA [18,19,20,21]. Similarly, L. draba, native to the Middle East and Mediterranean regions, particularly the Balkan Peninsula, Turkey, and Iran [22,23,24], has also become invasive in Europe [25], Australia, the USA, and Canada [26,27,28,29]. In contrast, the invasive L. campestre is native to Europe, where it experiences a more humid climate and sufficient rain supply [30,31].
The dispersal units in L. appelianum and L. draba are the whole fruit, as they are indehiscent fruit-producing plants, leading to germination directly from the pericarp (fruit coat) [32,33,34,35,36]. Conversely, seeds function as the dispersal units in L. campestre [30,31,35]. An interesting common characteristic among all the studied species is the tendency of the seeds to become mucilaginous upon wetting [33,37]. In addition, Mohammed et al. [34] observed that freshly harvested seeds and fruits of L. appelianum are non-dormant, while L. draba exhibits pericarp-mediated chemical dormancy, attributed to the inhibitory effect of abscisic acid (ABA) present in the fresh pericarp tissues. Similarly, Mohammed et al. [35] reported that L. campestre demonstrates physiological seed dormancy, a finding supported by Partzsch [31]. It is worth noting that after-ripening releases dormancy in both L. draba and L. campestre [34,35]. These studies were conducted under optimal germination conditions for the respective species. Furthermore, Mohammed and Mummenhoff [36] reported that the indehiscent fruit-producing L. appelianum and L. draba show stronger drought stress tolerance compared with the dehiscent fruit-producing L. campestre. However, the seed and fruit germination ecology under a broad range of temperature stress conditions remained largely unknown for these species. Therefore, we aim to conduct a comprehensive analysis of the germination behavior of seed and fruit populations, considering varying temperature conditions from 5 °C to 30 °C. Our goal is to identify the cardinal temperatures for seed and fruit germination, and to assess the potential invasiveness under future climate change of the three invasive Lepidium species: L. appelianum and L. draba, which produce indehiscent fruits, as well as L. campestre, which produces dehiscent fruits. We suppose that higher temperatures will lead to increased germination rates and percentages until it reaches the optimum temperature. However, it is anticipated that temperatures above the optimum could have a negative impact on seed germination. Considering the native distribution areas of the species, we hypothesize that seed and fruit germination of L. appelianum and L. draba may have a lower base temperature (very cold), but higher optimum and maximum temperatures (warm and hot). It is likely that these species exhibit a higher tolerance to broad range of temperatures, and we suggest that future climate change (global warming) may benefit them in comparison to L. campestre. Given the significant impact of noxious and invasive weeds on agriculture and biodiversity, understanding the ecological significance of dehiscent and indehiscent fruits is crucial for enhancing agricultural productivity and supporting biodiversity conservation efforts. Insights into the germination behaviors and adaptive strategies of these diaspore types can inform effective management practices to mitigate their negative effects on ecosystems and agricultural systems.

2. Materials and Methods

2.1. Seed Sources

Seeds for this study were obtained from mature fruits of L. appelianum Al-Shehbaz collected from 42.8° N, 69.9° E (Baydibek District, Kazakhstan), mature fruits of L. draba (L) collected from 39.5° N, 26.9° E (Burhaniye, Turkey), and mature seeds of L. campestre (L) W.T. Aiton collected from 56.8° N, 12.9° E (SJömossevägen, Halmstads kommun, Sweden). These seeds and fruits were mass propagated and collected from plants cultivated in the Botanical Garden of the University of Osnabrück, Germany. The fresh status of seeds and fruits was maintained by storing them at −20 °C until the experiments were initiated, following a protocol described by Baskin and Baskin [38].

2.2. Microscopy of Lepidium Fruit Morphology and Germinating Units

The fruit morphology and germinating units of three Lepidium species were examined, including the indehiscent fruit-producing species, L. appelianum and L. draba, as well as the dehiscent fruit-producing species, L. campestre. This analysis was quantified using a Leica M165 FC Fluorescence Classic stereomicroscope (Leica Microsystems, Switzerland) following methodologies outlined by Mohammed et al. [34], Lu et al. [39], and Sun et al. [40].

2.3. Seed and Fruit Material: Collection and Processing

Fresh seeds and fruits: Fresh mature seeds and fruits were collected directly from the mother plants immediately upon maturation. These freshly collected samples were air-dried at room temperature for seven days. The germination status of the seeds and fruits was assessed following the methods outlined by Baskin and Baskin [38] and Mohammed et al. [34] and stored in paper bags sealed within aluminum bags at −20 °C until the experiments were initiated. In contrast, after-ripened seeds and fruits were obtained by storing the fresh mature samples under laboratory conditions (25 ± 2 °C, 51% relative humidity) for four months, as per protocol established by Mohammed et al. [34].

2.4. Dormancy Characterization and Diaspore Types of the Three Lepidium Species

Previous studies have demonstrated that fresh L. draba fruits exhibit pericarp-mediated chemical dormancy [34], while fresh seeds of L. campestre exhibit non-deep physiological dormancy [35]. In contrast, fresh fruits and seeds of L. appelianum are classified as non-dormant [34]. The dormancy of L. draba seeds enclosed within indehiscent fruits and L. campestre seeds are effectively released after four months of after-ripening [34,35]. To break the dormancy of L. draba fruits and L. campestre seeds, the diaspores were stored under controlled laboratory conditions (25 ± 2 °C, 51% relative humidity) for a duration of four months, following the protocols established by Mohammed et al. [34] and Mohammed et al. [35]. In this study, we utilized the following materials: (A) fresh seeds and fruits of L. appelianum, (B) fresh seeds, fresh fruits, and after-ripened fruits of L. draba, and (C) both fresh and after-ripened seeds of L. campestre.

2.5. Germination Assessment of Isolated Seeds and Fruits Across Temperature Gradients

The germination assessment involved quantifying two types of dispersal units: isolated seeds (manually removed from the fruits by mechanically opening the pericarp) from L. appelianum and L. draba, and indehiscent fruits (true dispersal units), which consist of seeds enclosed within the pericarp. In contrast, isolated seeds, which serve as the dispersal units for L. campestre, were also utilized. A preliminary experiment was conducted to determine the germination temperature ranges for the species under investigation. The germination experiments were conducted using an automated 2D temperature gradient table (Flohr Instruments, Nieuwegein, The Netherlands) with a temperature range of 5 to 30 °C. Each germination assay included three technical replicates, with each replicate containing 25 seeds and 25 fruits as biological replicates, placed in 9 cm diameter Petri dishes lined with filter paper and moistened with 4 mL of distilled water. The germination assays were conducted under a 12/12 h light regime (white light at approximately 100 µmol m−2 s−1) at eight constant temperature regimes ranging from 5 to 30 °C. Isolated seeds and fruits (those containing seeds within the pericarp) were incubated for 4 weeks, with daily monitoring for germination. Germination was deemed complete when a visible protrusion of the radicle measuring 2 mm was observed, following the methods established by Baskin and Baskin [38], Mamut et al. [41], Tang et al. [42], Zhou et al. [43], and Mohammed et al. [34].

2.6. Data Analysis

A one-way ANOVA was conducted to examine the effect of different temperature treatments on the germination of the study species. Data were subjected to one-way ANOVA, with post hoc comparisons made by a Tukey’s honest significant difference test. The rejection threshold for all analyses was p < 0.05. Probit regression analysis was performed to determine the best fit between the actual and predicted germination values. The analysis processes the data to identify the maximum germination value at the earliest instance (based on the actual germination values). The results were visually represented using R version 4.3.2 (The R Foundation for Statistical Computing).

3. Results

3.1. The Indehiscent Fruit-Producing L. appelianum and L. draba Germinate Under a Broad Temperature Amplitude

The germination tests were conducted under eight temperature regimes ranging from 5 °C to 30 °C. Our findings indicate that the optimal temperature for the germination of freshly harvested fruits of L. appelianum is 23 °C (Figure 2). We observed an increasing germination percentage of fresh fruits of L. appelianum from 5 °C to 23 °C, indicating that this temperature falls within the sub-optimal range (Figure 2). At the optimal temperature for germination, approximately 90% germination percentage was achieved, demonstrating not only high germination percentage but also the highest speed of germination (Figure 2). These results suggest that fresh fruits of L. appelianum are non-dormant, as the germination percentage reached 90% under optimal germination conditions. Furthermore, the germination percentage declined above the optimum temperature, indicating that temperatures higher than the optimum are considered supra-optimal (Figure 2; Supplemental Figure S1A).
Fresh seeds of L. appelianum were manually isolated from the pericarp and demonstrated a high germination percentage (>90%) under the optimum temperature for the species, implying that they are non-dormant. The optimum germination temperature for isolated fresh seeds of L. appelianum was found to be 23.88 °C (Figure 2). This aligns with the optimal germination temperature for fresh fruits of L. appelianum shown in Figure 2, indicating a similar optimal temperature requirement for both enclosed seeds in the pericarp (fresh fruits) and isolated seeds. Additionally, the sub-optimal temperature range for fresh seeds of L. appelianum was identified as 5 °C to 23.88 °C, where germination increased until reaching the optimum temperature (Figure 2). Temperatures above the optimum are classified as supra-optimal, leading to a decrease in both the germination percentage and the rate of germination (Figure 2; Table 1; Supplemental Figure S1B).
Similarly to L. appelianum, the closely related indehiscent fruit-producing L. draba also exhibits an optimum temperature range for germination, which falls between 23 and 25 °C. Upon testing freshly harvested fruits of L. draba, a germination percentage of 60% was observed at the optimum germination temperature of 25 °C for this species (Figure 3). This result indicates the presence of dormancy in the freshly harvested fruits of L. draba. Both the germination percentage and the speed of germination decrease when transitioning from the optimum temperature to sub-optimal and supra-optimal temperatures (Figure 3).
Similarly to the freshly harvested fruits of L. draba, after-ripened fruits of L. draba exhibited successful germination at 25 °C, indicating that this temperature is optimal for the germination of after-ripened fruits of L. draba (Figure 3). At this temperature, a germination percentage of >85% (Table 2) was reported for after-ripened fruits of L. draba, signifying that after-ripening releases dormancy in the germination of L. draba fruits. The germination percentage and speed of germination decreased from the optimal temperature to sub-optimal and supra-optimal temperatures (Figure 3; Supplemental Figure S2B).
Manually isolated freshly harvested seeds of L. draba exhibited a germination rate of >90% at the optimum germination temperature (Figure 3, Table 2). The high germination percentage (>90%) suggests that isolated seeds of L. draba are non-dormant. For freshly harvested isolated seeds, the optimum germination temperature was found to be 23 °C. A comparison with the intact indehiscent fruit germination of L. draba revealed that isolated seeds of this species exhibit a slightly lower optimum temperature. The sub-optimal and supra-optimal temperature ranges were identified as 5–23 °C and 23–29.71 °C, respectively (Figure 3; Supplemental Figure S2C). In cases, the germination percentage and speed of germination decreased as the temperature deviated to either sub-optimal or supra-optimal extremes.

3.2. Impact of Temperature Stress on Germination Success of the Invasive Dehiscent Fruit-Producing L. campestre

The invasive dehiscent fruit-producing L. campestre demonstrated a preference for lower optimum temperatures compared to the indehiscent fruit-producing Lepidium species. Upon testing the freshly harvested seeds of L. campestre, a germination rate of approximately 60% was observed at the optimum temperature for germination, which was determined to be 16 °C (Figure 4, Table 2). Consequently, the optimal germination temperature for L. campestre is notably lower than that of the indehiscent fruit-producing L. appelianum and L. draba (23–25 °C). The recorded germination percentage (60%) of L. campestre fresh seeds indicates that the species exhibits some level of dormancy. Furthermore, the germination percentage was observed to decrease from the optimal to sub-optimal and supra-optimal temperatures (Figure 4; Supplemental Figure S3A).
The after-ripened seeds of L. campestre displayed a significantly high germination percentage (100%) compared to the freshly harvested seeds (60%) of the same species, indicating that after-ripening may release dormancy in this species (Table 2). The optimum temperature for the germination of after-ripened seeds of L. campestre was determined to be 18.44 °C (Figure 4, Supplemental Figure S3B), slightly higher than the optimum germination temperature of freshly harvested seeds (16 °C) of L. campestre. Additionally, the germination percentage and speed of germination were noted to decrease from the optimum temperature to sub-optimal and supra-optimal temperatures (Figure 4).

3.3. Germination Characteristics Reveal Temperature Stress Tolerance in Indehiscent Fruit-Producing Lepidium Species

The analysis revealed that freshly harvested fruits and seeds of L. appelianum exhibit notably low base temperatures (Tb) of 1 °C and 2.5 °C, respectively, compared to the base temperatures of L. draba seeds and fruits, as well as L. campestre seed germination (Table 1). Specifically, the base temperatures for germination of L. draba were determined to be 5.3 °C for freshly harvested fruits, 4.0 °C for after-ripened fruits, and 5.3 °C for freshly harvested isolated seeds (Table 1). In contrast, the base temperatures for L. campestre were found to be higher, at 6.0 °C for freshly harvested seeds and 5.8 °C for after-ripened seeds (Table 1).
Additionally, the maximum temperatures (Tc(50), where 50% germination occurs) for L. appelianum and L. draba are significantly higher (p < 0.001) than those of L. campestre (Table 1; Supplemental Figures S1–S3). The maximum temperature for 50% germination of freshly harvested fruits of L. appelianum was observed at 39.8 °C, while for freshly harvested manually isolated seeds, it was 35 °C (Table 1; Supplemental Figure S1A,B). In comparison, L. draba exhibited maximum germination temperatures (Tc(50)) of 33.8 °C, 34.4 °C, and 34.4 °C for freshly harvested fruits, after-ripened fruits, and freshly harvested manually isolated seeds, respectively (Table 1; Supplemental Figure S2A–C). Conversely, the dehiscent fruit-producing L. campestre displayed the lowest maximum temperatures (Tc(50)) for 50% germination, recording temperatures of 27.4 °C and 33.3 °C for freshly harvested seeds and after-ripened seeds, respectively (Table 1; Supplemental Figure S3A,B).

4. Discussion

4.1. Linking Indehiscent Fruit Development and Enhanced Temperature Stress Tolerance

Dehiscent fruits are the most common and likely the ancestral fruit type in Brassicaceae [46,47]. The transition of some plant species from dehiscent to indehiscent in fruit development could potentially be linked to the evolving adaptive traits, particularly in response to environmental stress factors [46,47]. Our research indicates that the indehiscent fruit-producing L. appelianum and L. draba exhibit significant temperature stress tolerance, especially during germination. These species develop non-fleshy, indehiscent fruits, where the fruit valves remain to enclose the seeds at dispersal, and the entire fruit acts as the dispersal unit [32,37,39,47,48]. This shift from dehiscent to indehiscent in fruit may be a crucial adaptation strategy, particularly in response to increased temperature stress. Our findings strongly support this hypothesis, as we observed that L. appelianum and L. draba, which produce indehiscent fruit, demonstrate greater temperature stress tolerance compared to L. campestre, which produces dehiscent fruit. This evidence suggests that the transition to indehiscent fruit production in certain species may be associated with an enhanced capacity to tolerate higher temperature stress during critical stages of development. These findings provide valuable insights into the ecological and adaptive significance of fruit type evolution in response to environmental stressors, particularly with regard to temperature stress, and contribute to our understanding of plant resilience in changing environmental conditions.

4.2. Wide Temperature Germination Range in L. appelianum and L. draba: An Adaptation to Extreme Climates

The seeds and fruits of L. appelianum and L. draba demonstrate a remarkable tolerance to very cold temperatures compared to L. campestre. The base temperature (Tb) for germination of L. appelianum seeds and fruits is reported to be between 1 °C and 2.5 °C, while for L. draba it ranges from 4 °C to 5.3 °C. In comparison, the base temperature for the germination of L. campestre falls within a range of 5.8 °C to 6.0 °C. This highlights the exceptional cold temperature tolerance of L. appelianum and L. draba, suggesting their ability to germinate under extremely cold conditions. Moreover, it is worth noting that L. appelianum and L. draba demonstrate a higher optimum temperature (To) for seed and fruit germination when compared to L. campestre. The optimum temperatures for seed and fruit germination of L. appelianum and L. draba fall within a range of 23 °C to 25 °C, while the optimum temperature (To) for the germination of L. campestre seeds is within 16 °C to 18 °C. These findings suggest that the indehiscent fruit-producing L. appelianum and L. draba display a higher optimal temperature for seed and fruit germination compared to L. campestre.
The higher tolerance to higher temperatures during seed and fruit germination in L. appelianum and L. draba is further supported by their maximum temperature for fifty percent germination (Tc(50)). The maximum temperature for fifty percent germination reveals that L. appelianum seeds and fruits germinate at higher maximum temperatures compared to L. draba. Specifically, the maximum temperature for fifty percent germination of seeds and fruits of L. appelianum ranges from 35 °C to 39.8 °C, while L. draba shows a maximum temperature for fifty percent seed and fruit germination of 33.8 °C to 34.4 °C. In comparison, L. campestre exhibits the least maximum temperature for fifty percent germination of seeds, ranging from 27.4 °C to 33.3 °C. This study highlights the wide temperature range within which the indehiscent fruits producing L. appelianum and L. draba seeds and fruits germinate, characterized by a very low base temperature and higher optimum and maximum temperatures, compared with the dehiscent fruit-producing L. campestre. Consequently, the indehiscent fruit-producing L. appelianum and L. draba display a higher temperature stress tolerance during seed and fruit germination compared to the dehiscent fruit-producing L. campestre.
The high temperature stress tolerance abilities of L. appelianum and L. draba can be attributed to their native distribution areas, showcasing their inherent adaptation to extreme continental, arid, and semiarid climates. L. appelianum, native to central Asia, inhabits arid regions in Kazakhstan, Uzbekistan, Turkmenistan, northern Iran, and Afghanistan, characterized by long, hot, dry summers and cold, dry winters [17,18,19]. Similarly, L. draba, native to central Asia and Siberia, including the Balkan Peninsula, Georgia, Armenia, Azerbaijan, Turkmenistan, Kazakhstan, southern Russia, Turkey, Israel, Syria, Iraq, and Iran, experiences a Mediterranean and continental-influenced climate, featuring warm summers but very cold and dry winters [18,22,23,24]. In contrast, L. campestre, native to Europe, is commonly found in the humid/humid nemoral zone with reliable and sufficient rainfall supply in countries across the Nordic region [16,30,31,49]. The distinct native habitats and climate preferences highlight the inherent adaptability of L. appelianum and L. draba to thrive in regions characterized by high temperature stress, indicating their potential for high temperature stress tolerance compared to L.campestre, which is better adapted to humid environments. These ecological insights underline the relevance of native habitat considerations in understanding the adaptive traits and stress tolerance capacities of plant species, thereby providing valuable information for assessing and managing plant populations in varying environmental conditions.

4.3. Distribution Patterns and Invasive Status: Implications for Management of Lepidium Species

The wide distribution of the indehiscent fruit-producing L. appelianum and L. draba in their introduced ranges, compared to the dehiscent fruit-producing L. campestre, raises significant ecological and agricultural concerns. L. appelianum and L. draba are widely distributed across continents, except Antarctica, presenting challenges for ecosystem management and agricultural practices [20,27,50,51]. L. appelianum has been reported in various countries, including Argentina, Australia, Canada, and the USA [18,52], but is not listed among established species in Europe [18,53]. Conversely, L. draba is most prevalent in arable land in Europe [18,25] and has become established as an agricultural weed in Canada, Australia, and the United States [18,50,51]. In the USA, Canada, and Australia, both L. appelianum and L. draba are classified as noxious and invasive weeds, posing significant challenges in terms of control and eradication [18]. In contrast, the distribution patterns of L. campestre suggest its invasive nature in regions with sufficient rainfall [30]. These findings suggest the need for continued monitoring and effective management strategies to mitigate the impact of the indehiscent fruit-producing invasive Lepidium species on ecosystems and agricultural practices. Furthermore, the wide distribution of L. appelianum and L. draba across diverse geographical regions further highlights their potential for broad temperature stress tolerance and adaptability, emphasizing the need for dedicated efforts to address their invasive tendencies and ecological impact.
The temperature stress tolerance observed in the indehiscent fruit-producing L. appelianum and L. draba may be a contributing factor to their invasiveness during seed germination. These species have been identified as significant noxious weeds, ranking 8th out of 45 in multiple noxious weed lists across the United States, Australia, and Canada, as documented by Skinner et al. [54], the USDA [28], and the Invaders Database System [55]. Research from Mulligan and Findlay [19], Francis et al. [50], and Mulligan [56] supports their infestation of agricultural land, pastures, riparian areas, and waste areas in these regions. In contrast, L. campestre has been noted to be invasive in areas within its distribution range that receive sufficient rainfall, as highlighted by Geleta et al. [16] and Montana Natural Heritage Program [49]. This study suggests that the broader temperature stress tolerance exhibited by the indehiscent fruit-producing L. appelianum and L. draba during germination may contribute to their invasive nature when compared to the dehiscent fruit-producing L. campestre.

4.4. Invasive Plant Traits, Temperature Stress, and the Success of Indehiscent-Fruited Lepidium Species

It is well documented that several characteristics of invasive plants could provide them with advantages over native species in response to climate change such as temperature stress. These include germination ecology and dormancy mechanisms; broader environmental tolerance; high competitiveness for resources; production of secondary metabolites; and long-distance dispersal capacity, as reported in studies by Baker [57], Daehler [58], Hellmann et al. [59], Whitney and Gabler [60], van Kleunen et al. [61], Clements and DiTommaso [62,63], and Wolkovich and Cleland [64]. These traits, which are more likely associated with seed germination, may indeed give invasive plants an advantage when adapting to environmental changes brought by climate change [65].

4.4.1. Germination Ecology and Dormancy Mechanisms as Drivers of Indehiscent-Fruited Lepidium Invasiveness Under Temperature Stress

In our study systems, we observed that the indehiscent fruit-producing L. appelianum and L. draba exhibit different dormancy characteristics in response to environmental factors. Freshly harvested seeds and fruits of L. appelianum show non-dormancy, whereas freshly harvested fruits of L. draba exhibit fruit coat-imposed chemical dormancy, which may confer a different level of tolerance to temperature stresses during seed and fruit germination [34]. Additionally, we found that freshly harvested seeds of L. campestre display physiological dormancy, adding another dimension to the variation in seed germination across species within the genus Lepidium [35]. These results emphasize the influence of geographical variation in environmental factors, such as temperature, on the dormancy and germination characteristics of Lepidium species, potentially leading to population differentiation. Moreover, the ability of introduced plants to rapidly adapt to local environments plays a crucial role in their expansion and invasion success in introduced ranges. Therefore, understanding the intraspecific variation in germination characteristics across geographic and environmental gradients is key to interpreting invasion mechanisms and predicting the distribution of exotic species in the future. We also recognize that invasive success hinges on the capacity of species to germinate in diverse environments and rapidly outcompete native flora. Therefore, the germination success and timing, as influenced by temperature, represent significant invasion traits that warrant further investigation [66,67]. Overall, this underlines the complex interplay between seed dormancy, germination characteristics, environmental factors, and invasive potential, offering valuable insights into the mechanisms driving the spread of colonizing species.

4.4.2. Indehiscent Fruits in Lepidium Species with Broad Temperature Tolerance Enhance Invasiveness

The findings suggest that the indehiscent fruit-producing L. appelianum and L. draba demonstrate higher tolerance to higher temperature stresses during seeds and fruit germination compared to the dehiscent fruit-producing L. campestre. This wider range of temperature tolerance displayed by L. appelianum and L. draba indicates their potential to adapt to future climate change and thrive in a broader environmental context. Consequently, these species could be better equipped to expand their range to higher elevations or latitudes in response to global warming, allowing for successful invasion of alien species [68,69,70]. Temperature emerges as a critical factor affecting plant invasion during seed germination, underscoring the significance of understanding species-specific responses to temperature changes in the context of invasive plant species.

4.4.3. High Competitiveness in Indehiscent Fruit-Producing Lepidium Species Increase Germination Success Under a Wider Range of Temperature Suggests Invasiveness

The higher tolerance of the indehiscent fruit-producing L. appelianum and L. draba to higher temperature stresses during seeds and fruit germination is evident. The broader range of temperature at which these species show seed and fruit germination suggests their high competitive ability, enhancing invasiveness under high-temperature conditions. Upon introduction to new environments, non-native species may aggressively compete with native biota for resources through interference competition as well as exploitation competition [71,72,73,74]. Recognizing that plants serve as the foundations of ecological communities, introduced plant species may pose a critical threat to ecosystems when they establish and become invasive [4,75].

4.4.4. Secondary Metabolites Could Promote Germination Success of Indehiscent Fruit-Producing Lepidium Species Under Temperature Stress Suggesting Invasiveness

Stress response promotes secondary metabolites’ production [76]. Indole glucosinolates are specific secondary metabolites of the Brassicaceae family derived from tryptophan, connected to auxin biosynthesis and involved in stress response [76,77]. It is imperative to underline the crucial impact of distinct glucosinolate patterns in Lepidium species. The high concentrations of specific glucosinolates, particularly the indole glucosinolates found in L. appelianum, strongly indicate their potential to thrive and become more invasive under changing climate conditions [35]. Conversely, L. campestre displays aliphatic glucosinolates, as reported by Mohammed et al. [35]. Furthermore, the isothiocyanates observed in L. draba, as documented by its ability to inhibit the germination and initial seedling growth of competing plant species, including wheat, barley, alfalfa, crested wheatgrass, bluebunch wheatgrass, and heart-podded hoary cress seeds, while also impeding the root length of these species [18,57,78], provide substantial evidence of its potential invasiveness under a global warming scenario. These findings suggest the significant role of secondary metabolites, such as glucosinolates, as contributors to the invasiveness of Lepidium species in various habitats facing environmental stresses.

4.4.5. Long-Distance Dispersal in Indehiscent Fruit-Producing Lepidium Species Could Indicate Invasiveness Under a Warming Climate

The impact of plant invasions on biodiversity and ecosystems has been widely recognized [79,80]. The increasing trend of these invasions is attributed to the facilitation of extra-range plant dispersal through globalization and the creation of new niche space due to human alterations of ecosystems [81,82]. In the studies conducted by Mummenhoff and Franzke [33] and Mohammed and Mummenhoff [37], the potential influence of dispersal mechanisms on the invasiveness and high-temperature stress tolerance during germination of indehiscent fruit-producing Lepidium species, such as L. draba, was highlighted. The differences in dispersal mechanisms between L. draba and L. campestre may contribute to their respective distribution patterns and invasive potential. L. draba’s higher potential for dispersal through water and wind indicates a broader dispersal range compared to L. campestre. This characteristic may aid in the colonization of diverse habitats and regions, suggesting a mechanism for coping with varying environmental conditions and potential temperature stress tolerance [37,83]. Furthermore, the strong adherence of L. campestre to sand particles suggests a more localized dispersal mechanism, resulting in seeds being transported shorter distances [37,84]. This localized dispersal mechanism may contribute to the species’ resilience in specific habitats. Understanding these distinct dispersal mechanisms and their implications on distribution patterns is crucial for predicting the spread of these invasive weed species in different habitats and regions, shedding light on their potential temperature stress tolerance and adaptability, especially for indehiscent fruit-producing species such as L. draba.

5. Conclusions

This study highlights the ecological and adaptive significance of fruit type evolution, specifically the transition from dehiscent to indehiscent fruits in Lepidium species, as a response to temperature stress tolerance. The findings reveal that the indehiscent fruit-producing L. appelianum and L. draba demonstrate remarkable temperature stress tolerance, particularly during germination, suggesting that this shift in fruit type is a crucial adaptation strategy in the face of increasing climate variability. L. appelianum and L. draba exhibit a wide germination temperature range, showcasing exceptional cold tolerance and higher optimum temperatures compared to L. campestre. This adaptation aligns with their native habitats in extreme continental and arid climates, further highlighting their potential for invasive success in diverse environments. The observed temperature stress tolerance among these species may considerably enhance their invasiveness, allowing them to successfully colonize new habitats and outcompete native flora including their dormancy mechanisms, competitive vigor, and ability for long-distance dispersal, supporting their capacity to thrive under changing environmental conditions. Therefore, understanding the interplay of these adaptive traits in L. appelianum and L. draba is critical for predicting their distribution patterns and invasive potential in response to climate change. These insights not only enhance our understanding of plant resilience but also inform effective management strategies for mitigating the ecological impacts of invasive species on native ecosystems.

Supplementary Materials

The following supporting information can be downloaded at https://www.mdpi.com/article/10.3390/agriculture15101078/s1, Supplemental Figure S1. Maximum temperature for 50% germination of Lepidium appelianum seeds and fruits. (A) Relative frequency of fresh fruits germination, showing a Tc(g) of approximately 39.8 °C. (B) Relative frequency of fresh seeds germination, with a Tc(g) of 35 °C.The maximum temperature for 50% germination of Lepidium appelianum ranges from 35 °C to 39.8 °C. The technique outlined by Soltani et al. [44]and Alvarado and Bradford [45] was followed to identify the maximum temperature for 50% fractional germination Tc(g). Supplemental Figure S2. Maximum temperature for 50% germination of Lepidium draba seeds and fruits. (A) Relative frequency of fresh fruits germination, showing a Tc(50) of approximately 33.8 °C. (B) Relative frequency of after-ripened fruits germination, with a Tc(50) of 34.4 °C. (C) Relative frequency of fresh seeds germination, with a Tc(50) of 34.4 °C. The maximum temperature for 50% germination of Lepidium draba ranges from 33.8 °C to 34.4 °C. The technique outlined by Soltani et al. [44] and Alvarado and Bradford [45] was followed to identify the maximum temperature for 50% fractional germination Tc(g). Supplemental Figure S3. Maximum temperature for 50% germination of Lepidium campestre seeds and fruits. (A) Relative frequency of fresh seeds germination, showing a Tc(50) of approximately 27.4 °C. (B) Relative frequency of after-ripened seeds germination, with a Tc(50) of 33.3 °C.The maximum temperature for 50% germination of Lepidium campestre ranges from 27.4 °C to 33.3 °C. The technique outlined by Soltani et al. [44] and Alvarado and Bradford [45] was followed to identify the maximum temperature for 50% fractional germination Tc(g).

Author Contributions

S.M. and K.M. planned and designed the research; S.M. performed experiments; S.M. and K.M. interpreted the data; S.M. and K.M. wrote the manuscript; both authors revised the final manuscript. Both authors have read and agreed to the published version of the manuscript.

Funding

This study was supported by the Deutsche Forschungsgemeinschaft, DFG (MU 1137/8-2) to K.M., Georg Förster Postdoctoral Research Grant (Alexander von Humboldt Stiftung) to S.M. We acknowledge support from the Open Access Publication Fund of the University of Tübingen.

Data Availability Statement

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

Acknowledgments

We thank Katja Tielbörger for hosting S.M., Alexander von Humboldt Foundation for a postdoctoral award to S.M., Ulrike Coja, Christoph Allgaier, Margret Ecke, and Annina Vollmer for technical assistance.

Conflicts of Interest

The authors declare no conflicts of interest.

References

  1. Finch-Savage, W.E.; Leubner-Metzger, G. Seed dormancy and the control of germination. New Phytol. 2006, 171, 501–523. [Google Scholar] [CrossRef] [PubMed]
  2. Kurtar, E.S. Modelling the effect of temperature on seed germination in some cucurbits. AJB 2010, 9, 1343–1353. [Google Scholar]
  3. Kirmizi, S. Dormancy and germination requirements of five species from Brassicaceae. JIST 2017, 7, 27–35. [Google Scholar] [CrossRef]
  4. Pham, D.H.; Wu, C.A. Seed longevity and germination of the emerging invasive species wavyleaf basketgrass (Oplismenus undulatifolius) under varied light regimes. Invasive Plant Sci. Manag. 2023, 16, 225–232. [Google Scholar] [CrossRef]
  5. Beckmann, M.; Bruelheide, H.; Erfmeier, A. Germination responses of three grassland species differ between native and invasive origins. Ecol. Res. 2011, 26, 763–771. [Google Scholar] [CrossRef]
  6. Heidari, Z.; Kamkar, B.; Sinaki, J.M. Influence of temperature on seed germination response of fennel. Adv. Plants Agric. Res. 2014, 1, 207–213. [Google Scholar]
  7. Weitbrecht, K.; Müller, K.; Leubner-Metzger, G. First off the mark: Early seed germination. J. Exp. Bot. 2011, 62, 3289–3309. [Google Scholar] [CrossRef]
  8. Channaoui, S.; El Idrissi, I.S.; Mazouz, H.; Nabloussi, A. Reaction of some rapeseed (Brassica napus L.) genotypes to different drought stress levels during germination and seedling growth stages. OCL 2019, 26, 23. [Google Scholar] [CrossRef]
  9. Lei, Y.H.; Chen, Z.P.; Li, Y.; Yu, Y.; Zhang, F.G.; Zhou, K.J.; Zhu, Z.H. Combined influence of low temperatureand drought on different varieties of rapeseed (Brassica napus L.). S. Afr. J. Bot. 2022, 147, 400–414. [Google Scholar]
  10. Chen, A.; Wang, Y.; Sui, X.; Jin, G.; Wang, K.; An, S. Effects of drought and temperature on the germination of seeds of Seriphidium transiliense, a desert xerophytic subshrub of Xinjiang, China. SST 2020, 48, 355–365. [Google Scholar] [CrossRef]
  11. Bhatt, A.; Chen, X.; Pompelli, M.F.; Jamal, A.; Mancinelli, R.; Radicetti, E. Characterizationof invasiveness, thermo tolerance and light requirement of nine invasive species in China. Plants 2023, 12, 1192. [Google Scholar] [CrossRef] [PubMed]
  12. Wen, B. Effects of high temperature and water stress on seed germination of the invasive species Mexican Sunflower. PLoS ONE 2015, 10, e0141567. [Google Scholar] [CrossRef] [PubMed]
  13. Al-Shehbaz, I.A. Lepidostemon (Brassicaceae) is no longer monotypic. Novon 2000, 10, 329–333. [Google Scholar] [CrossRef]
  14. Darbyshire, S.J.; Favreau, M.; Murray, M. Common and Scientific Names of Weeds in Canada; Publication 1397/B; Agriculture and Agri-Food Canada: Ottawa, ON, Canada, 2000; p. 132. [Google Scholar]
  15. Darbyshire, S.J. Inventory of Canadian Agricultural Weeds; Agriculture and Agri-Food Canada: Ottawa, ON, Canada, 2003; p. 396. [Google Scholar]
  16. Geleta, M.; Gustafsson, C.; Glaubitz, J.C.; Ortiz, R. High-density genetic linkage mappingof Lepidium based on genotyping-by-sequencing SNPs and segregating contig tag haplotypes. Front. Plant Sci. 2020, 11, 448. [Google Scholar] [CrossRef]
  17. Czerepanov, S.K. Vascular Plants of Russia and Adjacent States; Cambridge University Press: Cambridge, UK, 1995. [Google Scholar]
  18. Francis, A.; Warwick, S.I. The biology of Canadian weeds. 3. Lepidium draba L., L. chalepense L., and L. appelianum Al-Shehbaz (updated). Can. J. Plant Sci. 2008, 88, 379–401. [Google Scholar]
  19. Mulligan, G.A.; Findlay, J.N. The biology of Canadian weeds. 3. Cardaria draba, C. chalepensis, and C. pubescens. Can. J. Plant Sci. 1974, 54, 149–160. [Google Scholar]
  20. Gaskin, J.F.; Zhang, D.; Bon, M.C. Invasion of Lepidium draba (Brassicaceae) in the western United States: Distributions and origins of chloroplast DNA haplotypes. Mol. Ecol. 2005, 14, 2331–2341. [Google Scholar] [CrossRef]
  21. Gaskin, J.F. Clonal structure of invasive hoary cress (Lepidium draba) infestations. Weed Sci. 2006, 54, 428–434. [Google Scholar] [CrossRef]
  22. Mulligan, G.A.; Frankton, C. Taxonomy of the genus Cardaria with particular reference to the species introduced into North America. Can. J. Bot. 1962, 40, 1411–1425. [Google Scholar] [CrossRef]
  23. Ball, P.W. Cardaria. In Flora Europeae; Tutin, T.G., Heywood, V.H., Burges, N.A., Moore, D.M., Valentine, D.H., Walters, S.M., Webb, D.A., Eds.; Cambridge University Press: Cambridge, UK, 1964; p. 333. [Google Scholar]
  24. Goodwin, K. Biology, Ecology and Management of Whitetop (Cardaria spp.); Montana State University, MSU Extension: Bozeman, MT, USA, 2003. [Google Scholar]
  25. Hinz, H.L.; Cristofaro, M. Prospects for the Biological Control of Perennial Weeds; A Joint Report Prepared by CABI Bioscience Switzerland Centre and BBCA; CABI Bioscience Switzerland Centre and BBCA: Rome, Italy, 2005; p. 23. [Google Scholar]
  26. Scurfield, G. Cardaria draba (L.) Desv. (Lepidium draba L.). J. Ecol. 1962, 50, 489–499. [Google Scholar] [CrossRef]
  27. USDA. Hoary Cress Consortium; USDA ARS Northern Plains Agricultural Research Laboratory: Sidney, Australia, 2002.
  28. USDA. The Plants Database; National Plant Data Center: Baton Rouge, LA, USA, 2004.
  29. Rice, P. Invaders Database System. 2017. Available online: https://invader.dbs.umt.edu/ (accessed on 8 February 2025).
  30. Schroeder, F.G. Lehrbuch der Pflanzengeographie; Quelle and Meyer: Wiesbaden, Germany, 1998. [Google Scholar]
  31. Partzsch, M. Zur Keimungsbiologie acht ausgewählter kurzlebiger Ruderal und Segetalarten. Hercynia NF 2010, 43, 149–166. [Google Scholar]
  32. Al-Shehbaz, I.A. The genera of Lepidieae (Cruciferae; Brassicaceae), the southeastern United States. J. Arnold Arbor. 1986, 67, 265–311. [Google Scholar] [CrossRef]
  33. Mummenhoff, K.; Franzke, A. Gone with the bird: Late tertiary and quaternary intercontinental long-distance dispersal and allopolyploidization in plants. Syst. Biodivers. 2007, 5, 255–260. [Google Scholar] [CrossRef]
  34. Mohammed, S.; Turečková, V.; Tarkowská, D.; Strnad, M.; Mummenhoff, K.; Leubner-Metzger, G. Pericarp-mediated chemical dormancy controls the fruit germination of the invasive hoary cress (Lepidium draba), but not of hairy whitetop (Lepidium appelianum). Weed Sci. 2019, 67, 560–571. [Google Scholar] [CrossRef]
  35. Mohammed, S.; Bhattacharya, S.; Gesing, M.A.; Klupsch, K.; Theißen, G.; Mummenhoff, K.; Müller, C. Morphologically and physiologically diverse fruits of two Lepidium species differ in allocation of glucosinolates into immature and mature seed and pericarp. PLoS ONE 2020, 15, e0227528. [Google Scholar] [CrossRef]
  36. Mohammed, S.; Mummenhoff, K. Ecological Adaptations for Success: Indehiscence Fruits Promote Drought-Tolerant Germination in Invasive Lepidium Species. SSRN 2025. [Google Scholar] [CrossRef]
  37. Mohammed, S.; Mummenhoff, K. Functional divergence exists in mucilage-mediated seed dispersal, but not in germination of myxospermic Lepidium campestre and Lepidium draba (Brassicaceae). Acta Oecol. 2024, 125, 104042. [Google Scholar] [CrossRef]
  38. Baskin, C.C.; Baskin, J.M. Seeds: Ecology, Biogeography and Evolution of Dormancy and Germination; Academic Press: San Diego, CA, USA, 2014. [Google Scholar]
  39. Lu, J.J.; Tan, D.Y.; Baskin, J.M.; Baskin, C.C. Fruit and seed heteromorphism in the cold desert annual ephemeral Diptychocarpus strictus (Brassicaceae) and possible adaptive significance. Ann. Bot. 2010, 105, 999–1014. [Google Scholar] [CrossRef]
  40. Sun, Y.; Tan, D.Y.; Baskin, C.C.; Baskin, J.M. Role of mucilage in seed dispersal and germination of the annual ephemeral Alyssum minus (Brassicaceae). Aust. J. Bot. 2012, 60, 439–449. [Google Scholar] [CrossRef]
  41. Mamut, J.; Tan, D.Y.; Baskin, C.C.; Baskin, J.M. Role of trichomes and pericarp in the seed biology of the desert annual Lachnoloma lehmannii (Brassicaceae). Ecol. Res. 2014, 29, 33–44. [Google Scholar] [CrossRef]
  42. Tang, A.J.; Tian, M.H.; Long, C.L. Dormancy and germination in short-lived Lepidium perfoliatum L. (Brassicaceae) seeds. Pak. J. Bot. 2010, 42, 201–211. [Google Scholar]
  43. Zhou, Y.M.; Lu, J.J.; Tan, D.Y.; Baskin, C.C.; Baskin, J.M. Seed germination ecology of the colddesert annual Isatisviolascens (Brassicaceae): Two levels of physiologicaldormancy and role of the pericarp. PLoS ONE 2015, 10, e0140983. [Google Scholar] [CrossRef] [PubMed]
  44. Soltani, A.; Robertson, M.; Torabi, B.; Yousefi-Daz, M.; Sarparast, R. Modelling seedling emergence in chickpea as influenced by temperature and sowing depth. Agric.For. Meteorol. 2006, 138, 156–167. [Google Scholar] [CrossRef]
  45. Alvarado, V.; Bradford, K.J. A hydrothermal time model explains the cardinal temperatures for seed germination. Plant Cell Environ. 2022, 25, 1061–1069. [Google Scholar] [CrossRef]
  46. Mummenhoff, K.; Polster, A.; Mühlhausen, A.; Theißen, G. Lepidium as a model systemfor studying the evolution of fruit development in Brassicaceae. J. Exp. Bot. 2009, 60, 1503–1513. [Google Scholar] [CrossRef]
  47. Mühlhausen, A.; Lenser, T.; Mummenhoff, K.; Theißen, G. Evidence that an evolutionary transition from dehiscent to indehiscent fruits in Lepidium (Brassicaceae) was caused by a change in the control of valve margin identity genes. Plant J. 2013, 73, 824–835. [Google Scholar] [CrossRef]
  48. Cousens, R.D.; Young, K.R.; Tadayyon, A. The role of the persistent fruit wall in seed water regulation in Raphanus raphanistrum (Brassicaceae). Ann. Bot. 2010, 105, 101–108. [Google Scholar] [CrossRef]
  49. Montana Natural Heritage Program. Lepidium campestre (Field Pepper-Grass) Predicted Suitable Habitat Model; Montana Natural Heritage Program: Helena, MT, USA, 2024; p. 17. [Google Scholar]
  50. Francis, A.; Lujan-Toro, B.E.; Warwick, S.I.; Macklin, J.A.; Martin, S.L. Update on the Brassicaceae species checklist. Biodivers. Data. J. 2021, 9, e58773. [Google Scholar] [CrossRef]
  51. Mulligan, G.A. Weedy introduced mustards (Brassicaceae) of Canada. Can. Field-Nat. 2002, 116, 623–631. [Google Scholar] [CrossRef]
  52. Al-Shehbaz, I.A.; Mummenhoff, K.; Appel, O. Cardaria, Coronopus, and Stroganowia are united with Lepidium (Brassicaceae). Novon 2002, 12, 5–11. [Google Scholar] [CrossRef]
  53. Jalas, J.; Suominen, J.; Lampinen, R. (Eds.) Atlas Florae Europaeae distribution of vascular plants in Europe. Vol. 11: Cruciferae (Ricotia to Raphanus); Helsinki University Printing House: Helsinki, Finland, 1996; p. 310. [Google Scholar]
  54. Skinner, K.; Smith, L.; Rice, P. Using noxious weed lists to prioritize targets for developing weed management strategies. Weed Sci. 2000, 48, 640–644. [Google Scholar] [CrossRef]
  55. Invaders Database System. Noxious Weeds in the US and Canada; University of Montana: Missoula, MT, USA, 2006. [Google Scholar]
  56. Mulligan, G.A. Chromosome numbers determined from Canadian and Alaskan material of native and naturalized mustards, Brassicaceae (Cruciferae). Can. Field-Nat. 2002, 116, 611–622. [Google Scholar] [CrossRef]
  57. Baker, H.G. The evolution of weeds. Annu. Rev. Ecol. Syst. 1974, 5, 1–24. [Google Scholar] [CrossRef]
  58. Daehler, C.C. Performance comparisons of co-occurring native and alien invasive plants: Implications for conservation and restoration. Ann. Rev. Ecol. Evol. Syst. 2003, 34, 183–211. [Google Scholar] [CrossRef]
  59. Hellmann, J.J.; Byers, J.E.; Bierwagen, B.G.; Dukes, J.S. Five potential consequences of climate change for invasive species. Biol. Conserv. 2008, 22, 534–543. [Google Scholar] [CrossRef]
  60. Whitney, K.D.; Gabler, C.A. Rapid evolution in introduced species, ‘invasive traits’ and recipient communities: Challenges for predicting invasive potential. Divers. Distrib. 2008, 14, 569–580. [Google Scholar] [CrossRef]
  61. van Kleunen, M.; Dawson, W.; Schlaepfer, D.; Jeschke, J.M. Are invaders different? A conceptual framework of comparative approaches for assessing determinants of invasiveness. Ecol. Lett. 2010, 13, 947–958. [Google Scholar] [CrossRef]
  62. Clements, D.R.; DiTommaso, A. Climate change and weed adaptation: Can evolution of invasive plants lead to greater range expansion than forecasted? Weed Res. 2011, 51, 227–240. [Google Scholar] [CrossRef]
  63. Clements, D.R.; DiTommaso, A. Predicting weed invasion in Canada under climate change: Evaluating evolutionary potential. Can. J. Plant Sci. 2012, 92, 1013–1020. [Google Scholar] [CrossRef]
  64. Wolkovich, E.M.; Cleland, E.E. Phenological niches and the future of invaded ecosystems with climate change. AoB Plants 2014, 31, plu013. [Google Scholar] [CrossRef]
  65. Walck, J.L.; Hidayati, S.; Dixon, K.W.; Thompson, K.; Poschlod, P. Climate change and plant regeneration from seed. Glob. Change Biol. 2011, 17, 2145–2161. [Google Scholar] [CrossRef]
  66. Moravcova, L.; Pyšek, P.; Pergl, J.; Perglova, I.; Jarošík, V. Seasonal pattern of germination and seed longevity in the invasive species Heracleum mantegazzianum. Preslia 2006, 78, 287–301. [Google Scholar]
  67. Gioria, M.; Pyšek, P. Early bird catches the worm: Germination as a critical step in plant invasion. Biol. Invasions 2017, 19, 1055–1080. [Google Scholar] [CrossRef]
  68. Cunze, S.; Leiblein, M.C.; Tackenberg, O. Range expansion of Ambrosia artemisiifolia in Europe is promoted by climate change. Int. Sch. Res. 2013, 2013, 610126. [Google Scholar] [CrossRef]
  69. Allen, J.M.; Bradley, B.M. Out of the weeds? Reduced plant invasion risk with climate change in the continental United States. Biol. Conserv. 2016, 203, 306–312. [Google Scholar] [CrossRef]
  70. Panda, R.M.; Behera, M.D.; Roy, P.S. Assessing distributions of two invasive species of contrasting habits in future climate. J. Environ. Manage. 2018, 213, 478–488. [Google Scholar] [CrossRef]
  71. Bennett, A.E.; Thomsen, M.; Strauss, S.Y. Multiple mechanisms enable invasive speciesto suppress native species. Am. J. Bot. 2011, 98, 1086–1094. [Google Scholar] [CrossRef]
  72. Allstadt, A.; Caraco, T.; Molnár, F.; Korniss, G. Interference competition and invasion: Spatial structure, novel weapons and resistance zones. J. Theor. Biol. 2012, 306, 46–60. [Google Scholar] [CrossRef]
  73. Gioria, M.; Osborne, B.A. Resource competition in plant invasions: Emerging patterns and research needs. Front. Plant Sci. 2014, 5, 501. [Google Scholar] [CrossRef]
  74. Le Louarn, M.; Couillens, B.; Deschamps-Cottin, M.; Clergeau, P. Interference competition between an invasive parakeet and native bird species at feeding sites. J. Ethol. 2016, 34, 291–298. [Google Scholar] [CrossRef]
  75. Weidlich, E.W.A.; Flórido, F.G.; Sorrini, T.B.; Brancalion, P.H.S. Controlling invasive plant species in ecological restoration: A global review. J. Appl. Ecol. 2020, 57, 1806–1817. [Google Scholar] [CrossRef]
  76. Salehin, M.; Li, B.; Tang, M.; Katz, E.; Song, L.; Ecker, J.R.; Kliebenstein, D.J.; Estelle, M. Auxin sensitiveAux/IAA proteins mediate drought tolerance in Arabidopsis by regulating glucosinolate levels. Nat. Commun. 2019, 10, 4021. [Google Scholar] [CrossRef] [PubMed]
  77. Eom, S.H.; Baek, S.A.; Kim, J.K.; Hyun, T.K. Transcriptome analysis in chinese cabbage (Brassica rapa ssp. Pekinensis) provides the role of glucosinolate metabolism in response to drought stress. Molecules 2018, 23, 1186. [Google Scholar] [PubMed]
  78. Kiemnec, G.L.; McInnis, M.L. Hoary cress (Cardaria draba) root extract reduces germination and root growth of five plant species. Weed Technol. 2002, 16, 231–234. [Google Scholar] [CrossRef]
  79. Mack, R.N.; Simberloff, D.; Lonsdale, W.M.; Evans, H.; Clout, M.; Bazzaz, F.A. Biotic invasions: Causes, epidemiology, global consequences, and control. Ecol. Appl. 2000, 10, 689–710. [Google Scholar] [CrossRef]
  80. Pejchar, L.; Mooney, H.A. Invasive species, ecosystem services and human well-being. Trends Ecol. Evol. 2009, 24, 497–504. [Google Scholar] [CrossRef]
  81. Blois, J.L.; Zarnetske, P.L.; Fitzpatrick, M.C.; Finnegan, S. Climate change and the past, present, and future of biotic interactions. Science 2013, 341, 499–504. [Google Scholar] [CrossRef]
  82. Tilman, D.; Lehman, C. Human-caused environmental change: Impacts on plant diversity and evolution. Proc. Natl. Acad. Sci. USA 2001, 98, 5433–5440. [Google Scholar] [CrossRef]
  83. Mohammed, S.; Steinbrecher, T.; Leubner-Metzger, G.; Mummenhoff, K. Differential Primary Seed and Fruit Dispersal Mechanisms and Dispersal Biomechanics in Invasive Dehiscent and Indehiscent-Fruited Lepidium Species. Plants 2025, 14, 446. [Google Scholar] [CrossRef]
  84. Thiede, D.A.; Augspurger, C.K. Intraspecific variation in seed dispersion of Lepidium campestre (Barassicaceae). Am. J. Bot. 1996, 83, 856–866. [Google Scholar] [CrossRef]
Agriculture 15 01078 g001aAgriculture 15 01078 g001b
Figure 1. Comparative study on the fruit morphology and germinating units of the indehiscent fruit-producing L. appelianum and L. draba, in comparison to the dehiscent fruit-producing L. campestre. (I) illustrates the fruit morphology of the Lepidium species. (II) depicts the true dispersal units of the Lepidium species, noting that the entire fruit serves as a dispersal unit in L. appelianum and L. draba, while the seeds act as the dispersal unit in dehiscent fruit-producing L. campestre. It is observed that L. appelianum can germinate immediately as it does not exhibit dormancy. Contrastingly, fresh fruits of L. draba and fresh seeds of L. campestre demonstrate dormancy, which is released through after-ripening. (III) presents seed germination through pericarp rupture and manually isolated seeds from the pericarp in L. appelianum and L. draba, as well as seed germination of L. campestre. (IV) demonstrates the development of infructescence in the Lepidium species studied. Images were captured using the Leica FC Fluorescence Classic stereomicroscope (Leica Microsystems, Heerbrugg, Switzerland).
Figure 1. Comparative study on the fruit morphology and germinating units of the indehiscent fruit-producing L. appelianum and L. draba, in comparison to the dehiscent fruit-producing L. campestre. (I) illustrates the fruit morphology of the Lepidium species. (II) depicts the true dispersal units of the Lepidium species, noting that the entire fruit serves as a dispersal unit in L. appelianum and L. draba, while the seeds act as the dispersal unit in dehiscent fruit-producing L. campestre. It is observed that L. appelianum can germinate immediately as it does not exhibit dormancy. Contrastingly, fresh fruits of L. draba and fresh seeds of L. campestre demonstrate dormancy, which is released through after-ripening. (III) presents seed germination through pericarp rupture and manually isolated seeds from the pericarp in L. appelianum and L. draba, as well as seed germination of L. campestre. (IV) demonstrates the development of infructescence in the Lepidium species studied. Images were captured using the Leica FC Fluorescence Classic stereomicroscope (Leica Microsystems, Heerbrugg, Switzerland).
Agriculture 15 01078 g001aAgriculture 15 01078 g001b
Agriculture 15 01078 g002
Figure 2. The germination of L. appelianum fresh fruits and seeds throughout the course of time, as well as the actual and expected germination percentages. (A) The germination of L. appelianum fresh fruits throughout the course of time, as well as the actual and expected germination percentages. (a,c) L. appelianum fresh fruits germination percentages at sub-optimal and supra-optimal temperatures and (b,d) the difference between the expected and actual germination percentages at these two temperature ranges. The optimum temperature for the germination of L. appelianum fresh fruits is 23 °C. (B) The germination of L. appelianum fresh seeds throughout the course of time, as well as the actual and expected germination percentages. (a,c) L. appelianum fresh seeds germination percentages at sub-optimal and supra-optimal temperatures and (b,d) the difference between the expected and actual germination percentages at these two temperature ranges. For all the temperature treatments (n = 3 × 25), the germination tests were conducted over a period of four weeks. Probit regression analysis was performed to determine the best fit between the actual and predicted germination values. The analysis processes the data to identify the maximum germination value at the earliest instance (based on the actual germination values). The actual and predicted germination percentages show a great degree of resemblance when the R2 value is closer to 1. The optimum temperature for the germination of L. appelianum fresh seeds is 23.88 °C. Germination is considered completed when the visible radicle is about 2 mm.
Figure 2. The germination of L. appelianum fresh fruits and seeds throughout the course of time, as well as the actual and expected germination percentages. (A) The germination of L. appelianum fresh fruits throughout the course of time, as well as the actual and expected germination percentages. (a,c) L. appelianum fresh fruits germination percentages at sub-optimal and supra-optimal temperatures and (b,d) the difference between the expected and actual germination percentages at these two temperature ranges. The optimum temperature for the germination of L. appelianum fresh fruits is 23 °C. (B) The germination of L. appelianum fresh seeds throughout the course of time, as well as the actual and expected germination percentages. (a,c) L. appelianum fresh seeds germination percentages at sub-optimal and supra-optimal temperatures and (b,d) the difference between the expected and actual germination percentages at these two temperature ranges. For all the temperature treatments (n = 3 × 25), the germination tests were conducted over a period of four weeks. Probit regression analysis was performed to determine the best fit between the actual and predicted germination values. The analysis processes the data to identify the maximum germination value at the earliest instance (based on the actual germination values). The actual and predicted germination percentages show a great degree of resemblance when the R2 value is closer to 1. The optimum temperature for the germination of L. appelianum fresh seeds is 23.88 °C. Germination is considered completed when the visible radicle is about 2 mm.
Agriculture 15 01078 g002
Agriculture 15 01078 g003
Figure 3. The germination of L. draba fresh fruits, after-ripend fruits, and fresh seeds throughout the course of time, as well as the actual and expected germination percentages. (A) The germination of L. draba fresh fruits throughout the course of time, as well as the actual and expected germination percentages. (a,c) L. draba fresh fruits germination percentages at sub-optimal and supra-optimal temperatures and (b,d) the difference between the expected and actual germination percentages at these two temperature ranges. The optimum temperature for the germination of L. draba fresh fruits is 25 °C. (B) The germination of L. draba after-ripened fruits throughout the course of time, as well as the actual and expected germination percentages. (a,c) L. draba after-ripened fruits germination percentages at sub-optimal and supra-optimal temperatures and (b,d) the difference between the expected and actual germination percentages at these two temperature ranges. The optimum temperature for the germination of L. draba after-ripened fruits is 25 °C. (C) The germination of L. draba fresh seeds throughout the course of time, as well as the actual and expected germination percentages. (a,c) L. draba fresh seeds germination percentages at sub-optimal and supra-optimal temperatures and (b,d) the difference between the expected and actual germination percentages at these two temperature ranges. For all temperature treatments (n = 3 × 25), the germination tests were conducted over a period of four weeks. Probit regression analysis was performed to determine the best fit between the actual and predicted germination values. The analysis processes the data to identify the maximum germination value at the earliest instance (based on the actual germination values). The actual and predicted germination percentages show a great degree of resemblance when the R2 value is closer to 1. 23 °C is the optimum temperature for the germination of L. draba fresh seeds. Germination is considered completed when a 2 mm radicle is visible.
Figure 3. The germination of L. draba fresh fruits, after-ripend fruits, and fresh seeds throughout the course of time, as well as the actual and expected germination percentages. (A) The germination of L. draba fresh fruits throughout the course of time, as well as the actual and expected germination percentages. (a,c) L. draba fresh fruits germination percentages at sub-optimal and supra-optimal temperatures and (b,d) the difference between the expected and actual germination percentages at these two temperature ranges. The optimum temperature for the germination of L. draba fresh fruits is 25 °C. (B) The germination of L. draba after-ripened fruits throughout the course of time, as well as the actual and expected germination percentages. (a,c) L. draba after-ripened fruits germination percentages at sub-optimal and supra-optimal temperatures and (b,d) the difference between the expected and actual germination percentages at these two temperature ranges. The optimum temperature for the germination of L. draba after-ripened fruits is 25 °C. (C) The germination of L. draba fresh seeds throughout the course of time, as well as the actual and expected germination percentages. (a,c) L. draba fresh seeds germination percentages at sub-optimal and supra-optimal temperatures and (b,d) the difference between the expected and actual germination percentages at these two temperature ranges. For all temperature treatments (n = 3 × 25), the germination tests were conducted over a period of four weeks. Probit regression analysis was performed to determine the best fit between the actual and predicted germination values. The analysis processes the data to identify the maximum germination value at the earliest instance (based on the actual germination values). The actual and predicted germination percentages show a great degree of resemblance when the R2 value is closer to 1. 23 °C is the optimum temperature for the germination of L. draba fresh seeds. Germination is considered completed when a 2 mm radicle is visible.
Agriculture 15 01078 g003
Agriculture 15 01078 g004
Figure 4. The germination of L. campestre fresh and after-ripened seeds throughout the course of time, as well as the actual and expected germination percentages. (A) The germination of L. campestre fresh seeds throughout the course of time, as well as the actual and expected germination percentages. (a,c) L. campestre fresh seeds germination percentages at sub-optimal and supra-optimal temperatures and (b,d) the difference between the expected and actual germination percentages at these two temperature ranges. The optimum temperature for the germination of L. campestre fresh seeds is 16 °C. (B) The germination of L. campestre after-ripened seeds throughout the course of time, as well as the actual and expected germination percentages. (a,c) L. campestre after-ripened seeds germination percentages at sub-optimal and supra-optimal temperatures and (b,d) the difference between the expected and actual germination percentages at these two temperature ranges. For all the temperature treatments (n = 3 × 25), the germination tests were conducted over a period of four weeks. Probit regression analysis was performed to determine the best fit between the actual and predicted germination values. The analysis processes the data to identify the maximum germination value at the earliest instance (based on the actual germination values). The actual and predicted germination percentages show a great degree of resemblance when the R2 value is closer to 1. The optimum temperature for the germination of L. campestre after-ripened seeds is 18.44 °C. Germination is considered completed when the radicle protrusion (2 mm) is visible.
Figure 4. The germination of L. campestre fresh and after-ripened seeds throughout the course of time, as well as the actual and expected germination percentages. (A) The germination of L. campestre fresh seeds throughout the course of time, as well as the actual and expected germination percentages. (a,c) L. campestre fresh seeds germination percentages at sub-optimal and supra-optimal temperatures and (b,d) the difference between the expected and actual germination percentages at these two temperature ranges. The optimum temperature for the germination of L. campestre fresh seeds is 16 °C. (B) The germination of L. campestre after-ripened seeds throughout the course of time, as well as the actual and expected germination percentages. (a,c) L. campestre after-ripened seeds germination percentages at sub-optimal and supra-optimal temperatures and (b,d) the difference between the expected and actual germination percentages at these two temperature ranges. For all the temperature treatments (n = 3 × 25), the germination tests were conducted over a period of four weeks. Probit regression analysis was performed to determine the best fit between the actual and predicted germination values. The analysis processes the data to identify the maximum germination value at the earliest instance (based on the actual germination values). The actual and predicted germination percentages show a great degree of resemblance when the R2 value is closer to 1. The optimum temperature for the germination of L. campestre after-ripened seeds is 18.44 °C. Germination is considered completed when the radicle protrusion (2 mm) is visible.
Agriculture 15 01078 g004
Table 1. Comparative characterization of sub-optimal and supra-optimal temperatures among indehiscent fruit-producing L. appelianum and L. draba vs. dehiscent fruit-producing L. campestre. The base temperatures (Tb), standard deviation of the base temperature (σTb), maximum temperature for 50% germination (Tc(50)), and standard deviation of maximum temperature for 50% germination (σTc) were compared among the Lepidium species as a protocol outlined by Soltani et al. [44] and Alvarado and Bradford [45]. For all the temperature treatments (n = 3 × 25), the germination tests were conducted over a period of four weeks. Germination is considered completed when the radicle protrusion (2 mm) is visible.
Table 1. Comparative characterization of sub-optimal and supra-optimal temperatures among indehiscent fruit-producing L. appelianum and L. draba vs. dehiscent fruit-producing L. campestre. The base temperatures (Tb), standard deviation of the base temperature (σTb), maximum temperature for 50% germination (Tc(50)), and standard deviation of maximum temperature for 50% germination (σTc) were compared among the Lepidium species as a protocol outlined by Soltani et al. [44] and Alvarado and Bradford [45]. For all the temperature treatments (n = 3 × 25), the germination tests were conducted over a period of four weeks. Germination is considered completed when the radicle protrusion (2 mm) is visible.
Fruit TypesSpeciesDiaspore TypesSub-Optimal TemperaturesSupra-Optimal Temperatures
Tb(σTb)Tc(50)(σTc)
Indehiscent fruitsLepidium appelianumFresh fruits1.00.3539.80.34
Fresh seeds2.50.33350.32
Lepidium drabaFresh fruits5.31.2833.80.25
After-ripened fruits4.01.034.40.34
Fresh seeds5.30.2534.40.32
Dehiscent fruitsLepidium campestreFresh seeds6.00.2627.41.8
After-ripened seeds 5.80.1933.30.26
Table 2. Mean germination percentage of seeds and fruits from the indehiscent fruit-producing Lepidium appelianum and Lepidium draba, as well as seeds from the dehiscent fruit-producing Lepidium campestre. The mean ± SE (n = 3 × 25) for the species was determined under a broader temperature ranges of 5 °C to 30 °C, with germination tests conducted over a period of four weeks for all temperature treatments. Different letters (a–e) within species indicate statistically significant differences in mean values, determined by the Tukey pairwise multiple comparison test (p < 0.05). Germination is considered completed when the radicle protrusion (2 mm) is visible.
Table 2. Mean germination percentage of seeds and fruits from the indehiscent fruit-producing Lepidium appelianum and Lepidium draba, as well as seeds from the dehiscent fruit-producing Lepidium campestre. The mean ± SE (n = 3 × 25) for the species was determined under a broader temperature ranges of 5 °C to 30 °C, with germination tests conducted over a period of four weeks for all temperature treatments. Different letters (a–e) within species indicate statistically significant differences in mean values, determined by the Tukey pairwise multiple comparison test (p < 0.05). Germination is considered completed when the radicle protrusion (2 mm) is visible.
SpeciesSeed/Fruit TypeTemperature (°C)Germination (%) Mean ± S.E.
Lepidium appelianumFresh fruits5.000 ± 0.0 b
12.9650 ± 2.8 c
17.2565 ± 2.8 cd
20.2875 ± 5.7 d
23.0088 ± 1.6 a
25.1790 ± 2.7 a
27.8780 ± 5.7 ad
29.7175 ± 2.8 ad
Fresh seeds5.0010.5 ± 2.4 b
12.6250 ± 2.7 c
17.0765 ± 5.6 ac
20.2775 ± 5.4 ad
21.9485 ± 2.8 ad
23.8891 ± 5.7 d
26.8685 ± 5.4 d
29.0180 ± 2.5 ad
Lepidium drabaFresh fruits5.004 ± 0.5 b
12.8425 ± 2.6 a
17.2135 ± 2.4 ac
20.7040 ± 2.3 ac
23.0745 ± 2.5 c
25.0060 ± 5.4 cd
27.5845 ± 5.5 cd
29.5740 ± 5.3 acd
After-ripened fruits5.000 ± 0.0 b
12.8436 ± 5.6 c
17.2152 ± 5.4 ac
20.7066 ± 3.7 a
23.0772 ± 4.0 ad
25.0081 ± 3.1 d
27.5878 ± 5.0 d
29.5776 ± 3.4 d
Fresh seeds5.000 ± 0.0
12.9650 ± 2.3 b
17.2565 ± 2.7 cd
20.2878 ± 4.4 a
23.0091 ± 1.0 e
25.1785 ± 2.8 ae
27.8780 ± 2.4 ae
29.7175 ± 1.7 ad
Lepidium campestreFresh seeds5.002.6 ± 0.3 b
9.0041 ± 1.6 c
16.0057 ± 1.4 d
19.0037 ± 1.4 c
22.0031 ± 1.0 e
25.0021 ± 1.6 a
27.0019 ± 0.8 a
30.0017 ± 1.4 a
After-ripened seeds5.0020 ± 2.8 b
12.0550 ± 5.5 c
14.6590 ± 2.6 ae
18.44100 ± 0.0 ae
22.6885 ± 0.0 ae
25.1380 ± 2.7 a
27.6775 ± 2.7 ac
29.9860 ± 5.5 c
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

Mohammed, S.; Mummenhoff, K. Germination Under Temperature Stress Facilitates Invasion in Indehiscent Lepidium Species. Agriculture 2025, 15, 1078. https://doi.org/10.3390/agriculture15101078

AMA Style

Mohammed S, Mummenhoff K. Germination Under Temperature Stress Facilitates Invasion in Indehiscent Lepidium Species. Agriculture. 2025; 15(10):1078. https://doi.org/10.3390/agriculture15101078

Chicago/Turabian Style

Mohammed, Said, and Klaus Mummenhoff. 2025. "Germination Under Temperature Stress Facilitates Invasion in Indehiscent Lepidium Species" Agriculture 15, no. 10: 1078. https://doi.org/10.3390/agriculture15101078

APA Style

Mohammed, S., & Mummenhoff, K. (2025). Germination Under Temperature Stress Facilitates Invasion in Indehiscent Lepidium Species. Agriculture, 15(10), 1078. https://doi.org/10.3390/agriculture15101078

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