Next Article in Journal
New Data on the Distribution and Systematic Position of Marsupella minutissima, a Poorly Known Species from Gymnomitriaceae (Marchantiophyta)
Previous Article in Journal
Integrated Analysis of microRNAs and Transcription Factor Targets in Floral Transition of Pleioblastus pygmaeus
Previous Article in Special Issue
Influence of Habitat and Effects of Salt Stress on Biochemical and Physiological Parameters of Glycyrrhiza uralensis
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Plants
Volume 13
Issue 21
10.3390/plants13213035
plants-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

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

Phenological and Fungal Interactions of Malesherbia auristipulata Ricardi (Passifloraceae) in the Atacama Desert: Adaptations and Conservation in an Extreme Ecosystem

by
German F. Sepúlveda Chavera
1,*,
Eliana Belmonte Schwarzbaum
2,
Nicolas Valderrama Saez
1,
Mabel Arismendi Macuer
1 and
Wilson Huanca-Mamani
1
1
Departamento de Recursos Ambientales, Facultad de Ciencias Agronómicas, Universidad de Tarapacá, Avda. General Velásquez 1775, Arica 100190, Chile
2
Departamento de Biología, Facultad de Ciencias, Universidad de Tarapacá, Avda. General Velásquez 1775, Arica 100190, Chile
*
Author to whom correspondence should be addressed.
Plants 2024, 13(21), 3035; https://doi.org/10.3390/plants13213035
Submission received: 10 September 2024 / Revised: 21 October 2024 / Accepted: 28 October 2024 / Published: 30 October 2024
(This article belongs to the Special Issue Adaptive Strategies of Plants to Stress Factors)
Browse Figures
Review Reports Versions Notes

Abstract

:
Malesherbia auristipulata is an endemic plant species of the Atacama Desert, with unique morphological and physiological adaptations. This research was conducted at Cuesta El Águila, Arica and Parinacota Region, Chile. Adult and juvenile plants were monitored, recording their growth, flowering, and fruiting phases. Additionally, plant community species were identified. For the study of endophytic mycoflora, samples of seeds, roots, stems, and leaves were collected, disinfected, and cultivated in specific media. The isolated fungi were analyzed morphologically and molecularly, determining their distribution in different plant organs. The diversity of endophytic fungi associated with M. auristipulata and the associated fungal community was determined. The presence of endophytic fungi varied depending on the organ studied, suggesting dynamic interactions in the structure of its fungal community. Among the identified endophytic fungi, Alternaria sorghi, A. alstroemeriae, and Fusarium nurragi stand out for their presence in the root and stem of the plant. Of particular interest is the presence of F. circinatum in the leaves. This study provides valuable information for the conservation of M. auristipulata and other organisms in the Atacama Desert, highlighting the importance of ecological interactions in the resilience of plants to extreme environmental conditions.

1. Introduction

The Atacama Desert is recognized as one of the driest and most extreme environments on the planet, hosting a unique biodiversity that has developed exceptional adaptations to survive under severe environmental conditions [1,2,3]. The aridity of this region is attributed to a combination of geographic and climatic factors, such as the Humboldt Current and the orographic shadow created by the Andes, which block the entry of moisture [4]. This desert serves as an ideal natural laboratory for studying biological adaptation and ecological resilience. The species inhabiting the Atacama Desert have developed extraordinary mechanisms to store water and withstand intense ultraviolet radiation. A prominent example is Malesherbia auristipulata, an endemic plant with remarkable morphological and physiological adaptations, such as reduced leaves and thick cuticles that minimize water loss, as well as a deep root system that allows water extraction from the deepest layers of the soil [5,6].
Cuesta El Águila is the only place in Chile where the population of Malesherbia auristipulata has been described (Figure 1), extending at an altitude between 1810 and 1834 m above sea level. This area is part of the Sierra de Huaylillas, whose elevations range from 1540 to 2000 m, and was originated during the late Oligocene and early Miocene [7,8]. The region is characterized by extreme aridity, with an average annual precipitation of only 50 mm [9]. Precipitation at higher altitudinal levels is concentrated during the summer months, which increases the relative humidity of the air between late October and March [10]. Additionally, this region is vulnerable to flash floods caused by heavy rains, such as the one that occurred in January–February 2019 [11]. Despite its adaptations to the extreme environment of the Atacama Desert, M. auristipulata faces significant threats due to habitat loss and degradation. In Chile, this species was initially classified as rare [12]. It is currently listed as critically endangered [13], considering that the only known population in Chile occupies a very isolated basin and faces significant current and potential threats, including habitat degradation due to anthropogenic factors.
Phenology, which refers to the life cycles and the timing of plant interactions with their environment, is a crucial aspect for understanding the ecology of arid ecosystems. In the Atacama Desert, the phenology of M. auristipulata is closely linked to precipitation patterns and water availability. The synchronization of flowering and fruiting with rainfall events is fundamental for the reproductive success of plants in this extreme environment [14]. In this context, filamentous endophytic fungi, which live within plant tissues without causing apparent harm, play an essential role in the phenology and adaptation of plants to adverse environmental conditions [15,16]. Recent studies have shown that these fungi can enhance plant resistance to drought and diseases, directly influencing their survival and reproductive success [17,18]. Additionally, these microorganisms modify nutrient absorption and water use efficiency in plants [19].
The interaction between M. auristipulata and endophytic fungi is an emerging area of research that provides valuable insights into the adaptation strategies of plants in extreme environments. It has been demonstrated that endophytic fungi not only improve tolerance to abiotic stress but also influence plant resistance to pathogens [20]. Their presence in M. auristipulata is key to explaining its survival capability in one of the driest deserts in the world. However, little is still known about the specific relationship between the phenology of M. auristipulata and the diversity of filamentous fungi in the Atacama Desert.
This study presents results on the diversity of filamentous fungi associated with M. auristipulata at different phenological stages of the plant. Through field sampling techniques and molecular analysis, the taxonomic composition and relative abundance of these fungi were characterized in different parts of the plant, as well as in the surrounding substrate. Additionally, the correlation between the phenology of M. auristipulata and the structure of its associated fungal community was evaluated, with the aim of better understanding plant–fungi interactions in this extreme ecosystem and their relevance for the adaptation and conservation of species in the Atacama Desert.

2. Results and Discussion

2.1. Surrounding Plant Species in Its Natural Habitat

The distribution of the plant community M. auristipulata, classified according to their botanical family and geographic distribution in Chile, is presented in Table 1 [19]. It is important to note that no introduced species were found in the study area, which underscores the ecological integrity of this habitat. All recorded species are xerophytes, adapted to conditions of extreme aridity, and a significant proportion of them are endemic, which reinforces the uniqueness and conservation value of this ecosystem. The species are detailed according to their botanical family, specifying whether they are native or endemic, as well as their geographic distribution across different regions of the country. This information is crucial for understanding the floristic composition and ecological adaptations of the plant community in this arid ecosystem.
The plant community M. auristipulata is composed of 18 species, of which 8 are endemic and 10 are native. The distribution of these species by family is as follows: Aizoaceae (1 species), Asteraceae (4 species), Chenopodiaceae (2 species), Fabaceae (1 species), Malvaceae (2 species), Montiaceae (1 species), Nyctaginaceae (1 species), Passifloraceae (1 species), Solanaceae (4 species), and Verbenaceae (1 species). It is noteworthy that no introduced species were found in the study area, which is consistent with previous studies [5,20] (Figure 2).
Several plant families were observed, with the Solanaceae family standing out, comprising four species and a total of 723 individuals (674 of Nolana rhombifolia, 37 of Reyesia juniperoides, 7 of Solanum peruvianum, and 5 of Exodeconus flavus). This family is clearly dominant in the community. The Asteraceae family is also notable, with three recorded species and a total of 118 individuals (55 of Ambrosia artemisioides, 47 of Senecio zapahuirensis, and 16 of Trixis cacalioides).
The total number of individuals recorded at 49 sampling points along a 20 m linear transect highlights the abundance of different species. A total of 18 species were registered, indicating significant diversity in the studied area. The most abundant species was Nolana rhombifolia, with 674 individuals, representing approximately 51% of the total individuals recorded (1,319). Malesherbia auristipulata ranked second with 385 individuals, accounting for roughly 29% of the total. Species such as Tarasa operculata, Glandularia gynobasis, and Tetragonia microcarpa had only one individual each, suggesting they are less common in the area. The distribution is uneven, with the two most abundant species comprising over 80% of the total individuals. This suggests that these species either have competitive advantages in the habitat or that the environmental conditions favor their growth. The predominance of a few species could have implications for ecosystem health, as ecosystems with high diversity tend to be more resilient to environmental changes and disturbances. The low abundance of other species may indicate potential issues with local biodiversity, warranting further monitoring or conservation measures.
In environments with harsh conditions, some species can facilitate the growth of others. For instance, species like Atriplex glaucescens might create a microhabitat that benefits other plants by providing shade or retaining moisture in the soil. On the other hand, some species may engage in mutualistic relationships. For example, certain plants, like Malesherbia, can interact with fungi or other microorganisms (as discussed later) that help them absorb nutrients in exchange for sugars produced through photosynthesis, or by activating defense mechanisms. These interactions are well documented in the scientific literature, with numerous examples available.

2.2. Phenological Study of Malesherbia auristipulata in Its Natural Habitat

The annual phenology of M. auristipulata plants in Cuesta El Águila reveals the phenological events throughout the year, such as flowering, fruiting, and other life cycles, suggesting a seasonal phenological trend and its relationship with environmental factors, such as altitude and geographical location [9].
Table 2 presents a monthly phenological record, detailing the growth stages of M. auristipulata, documenting the different phenological stages throughout the year, and providing a detailed view of its life cycle in relation to the specific environmental conditions of the region. It allows a comparative analysis of adult and juvenile plants, providing information on their ability to adapt to changing environmental conditions as well as about the vegetation’s resilience when facing natural disasters.
Throughout the year, juvenile plants are predominantly in a vegetative state, especially in the early months, with 100% in the vegetative state in January. As the months progress, a slight increase in flowering and fruiting phases is observed, reaching a peak in August and September (13% in flowering and 8.7% in fruiting). Latency begins to increase in October, reaching 17.4% in November, while the vegetative state gradually decreases. In the case of adult plants, greater phenological variability is observed throughout the year. At the beginning, the majority remain in a vegetative state (68.4% in January), with a small percentage flowering and fruiting. The flowering and fruiting phases increase significantly between June and September, reaching a peak of fruiting in July (47.4%) and flowering in August (26.3%). Toward the last months of the year, latency increases while the percentage of plants in the vegetative and fruiting states decreases.

2.3. Endophytic Fungi Associated with Malesherbia auristipulata

The study of the diversity of endophytic fungi associated with Malesherbia auristipulata is based on their genetic identity, morphological characteristics of the colonies, taxonomically valuable structures, and their presence in different parts of the plant, such as the root, stem, and leaf. This information is crucial for understanding the possible implications of these fungi on the health of the plant and its ability to adapt to the environment. Additionally, Table 3 presents the identification of endophytic fungi species using the BLASTN bioinformatics tool [21]. This algorithm compares the DNA sequences of the fungi with a database to find the most similar sequence, allowing for species determination. The percentage of identity (% Identity) reflects the similarity between the DNA sequence of the endophytic fungi and the reference sequences stored in databases like NCBI. A higher percentage of identity indicates a greater similarity between the compared sequences [22]. Furthermore, Table 3 indicates the presence of endophytic fungi in different parts of the plant (M. auristipulata), such as the root, stem, and leaf. The presence of fungi in a specific sample is indicated by a “+” mark, while the absence of this mark indicates that no fungi were detected in that part of the plant. This detection method is commonly used in plant microbiota studies and has proved to be very efficient in identifying fungal colonization patterns in different plant tissues [16].
The data reveal a community of endophytic fungal species found in multiple samples and in different parts of the plant. Some fungi, such as Alternaria sorghi, A. alstroemeriae, and Fusarium nurragi, exhibit distribution in both the stem and root; Aureobasidium melanogenum is found only in the stem, and Fusarium circinatum only in the leaf. This pattern could be influenced by factors such as the plant’s genetic variability, soil composition, and environmental conditions [23]. The level of identity between species and isolates is variable. For example, Alternaria sorghi NR_160246.1 presents an identity range that varies between 99.13% and 99.83%, indicating a high genetic similarity among different isolates of this species. This phenomenon is consistent with what is expected in population genetics studies, where isolates of the same species usually show a high genetic relationship even in different environments [15]. These authors reported that Alternaria species are common in similar environments. Studying plant microbiota is fundamental for understanding plant–fungi interactions and their impact on plant health and adaptation to their environment [17].
The diversity of endophytic fungal species present in the analyzed sample, including genera such as Alternaria, Fusarium, and Aureobasidium, among others, is clearly reflected in Table 3. This taxonomic variability can be considered an indication of the complexity and health of the plant ecosystem studied [17] (Figure 3).
The phenological cycle of Malesherbia auristipulata, showing that juvenile plants remain mostly in the vegetative state throughout the year, while adult plants exhibit greater phenological changes, especially during the winter and spring periods, when fruiting and flowering increase (Figure 4).
The diversity in the morphology of the colonies of endophytic fungi obtained from A. auristipulata, on APD and 10 days of incubation at 22 ± 2 °C represents the richness of microorganisms associated with plants in desert environments, as manifested in this case (Figure 5).
The study of the relationship between phenology, plant community, and endophytic fungi provides a comprehensive view of the dynamics and health of ecosystems, with a specific focus on Malesherbia auristipulata [24]. The results of this research generate new hypotheses about how the phenology of endemic plants might influence the availability of resources for the surrounding flora and endophytic fungi [16,25]. For example, the flowering and fruiting period of M. auristipulata could affect the availability of pollen and nectar for pollinators, which in turn could impact the distribution and phenology of other plants in the community [26,27]. Additionally, the plant community in the same habitat as M. auristipulata could influence its phenology and vice versa through competition for resources such as light, water, and nutrients [28]. These types of plant–plant and plant–fungi interactions are fundamental for understanding the ecology of arid ecosystems and can have significant implications for biodiversity conservation and the management of these unique habitats [29].
Another hypothesis suggests that endophytic fungi can have significant effects on the phenology and health of host plants. Some of these fungi may promote plant growth and resistance to diseases, while others may act as pathogens or have neutral effects [19,30]. Therefore, the presence of certain endophytic fungi in Malesherbia auristipulata could influence its phenology and its interactions with the plant community [17,29].
It is important to consider that extreme events can have both short-term and long-term effects on phenology, the composition of the plant community, and the diversity of endophytic fungi in the ecosystem. These events can alter interactions between plants, and between plants and fungi, affecting the health and dynamics of Malesherbia auristipulata populations and other species in the region [31,32]. Such changes could significantly modify the structure and function of the ecosystem, highlighting the importance of understanding ecological interactions and the resilience of species in the face of extreme climatic events [29].
This study highlights the complexity of the relationships between phenology, plant community, and endophytic fungi and how these interactions can influence the structure and function of the ecosystems where Malesherbia auristipulata is found. A detailed analysis of these interactions provides valuable information for the conservation and management of this ecosystem [33,34]. Furthermore, it emphasizes the importance of understanding the dynamics of microbes, both in natural environments and in their relationship with host organisms, which enhances our appreciation of microbial diversity and its crucial role in terrestrial ecosystems [35,36].
Microbes are ubiquitous on Earth and possess the ability to survive in a wide variety of environments, ranging from hydrothermal vents in the deep ocean to deserts and polar regions [34]. Their ability to colonize even plant trichomes underscores the remarkable adaptability and diversity of microbes in different ecological niches [37].
Trichomes originate from epidermal cells and develop on the surface of various plant organs. These trichomes not only serve physical functions, such as protecting the plant against herbivores and increasing its stress tolerance (Figure 1D) [38,39,40], but they can also serve as habitats and infection sites for a variety of microbes, including saprophytic and pathogenic fungi [15].
The associations between fungi and plant trichomes have been the subject of a growing number of studies, which have revealed that trichomes can facilitate the adhesion and growth of fungi on the plant surface, creating a microenvironment conducive to their development [41]. These interactions can have significant implications for plant health and disease dynamics. An example of this is Tea Anthracnose, where the pathogenic fungus infects the plant through foliar trichomes, causing the characteristic leaf spots [42].
The case of Malesherbia auristipulata compared to other species, such as Pinus pinaster, shows how the relationship between the plant and the fungus Fusarium circinatum can vary significantly, from symbiosis to a pathogenic interaction. In M. auristipulata, F. circinatum appears to behave symbiotically without causing visible damage to the plant, suggesting that both species have developed an adaptive balance in the extreme environment of the Atacama Desert. However, in introduced species such as P. pinaster, F. circinatum acts as an aggressive pathogen, responsible for pitch canker, a serious disease affecting forest plantations [43]. In these pines, starting from the fourth day post-inoculation, the fungus begins to colonize the tissues, triggering a series of phytohormonal responses, including alterations in the levels of jasmonic acid (JA), salicylic acid (SA), ethylene (ET), and auxins, which facilitate the invasion of the pathogen [44,45]. These hormonal changes inhibit the plant’s natural defenses, allowing the fungus to spread and effectively damage the host tissue [45].
The study of the diversity of endophytic fungi associated with Malesherbia auristipulata is based on their genetic identity, morphological characteristics, and their presence in different plant organs such as the root, stem, and leaf. Recent research, including the morpho-molecular characterization of endophytic fungi from traditional medicinal plants like Adhatoda vasica and Cassia alata, highlights the effectiveness of ITS sequencing for identifying fungal species and understanding their ecological roles [46]. These fungi play a significant role in the plant’s adaptation to the extreme conditions of the Atacama Desert. By improving water retention, nutrient absorption, and plant defense mechanisms, endophytic fungi are crucial for survival in harsh environments [15,16].
In addition to facilitating plant growth and tolerance to drought, endophytic fungi also contribute to broader ecological interactions within plant communities. Studies have shown that fungi such as Alternaria and Fusarium, which were found in M. auristipulata, play important ecological roles in mitigating the effects of pathogens [17]. This symbiotic relationship helps explain the persistence of M. auristipulata in an ecosystem where the availability of water and nutrients is limited [27].
Furthermore, recent studies on the functional roles of these endophytic fungi provide a clearer understanding of their contributions to plant health and ecosystem stability. For example, Fusarium circinatum and Alternaria species found in this study have been shown to play roles in enhancing plant growth and protecting against biotic stressors [30]. The presence of these fungi in various plant organs suggests that they may have organ-specific functions, with some focusing on nutrient uptake from the roots, while others aid in defense in the stems and leaves.
Recent research on Amaranthus tricolor has demonstrated that different plant phenotypes can recruit distinct microbial communities in the rhizosphere, suggesting a strong influence of plant traits on microbial assembly [47]. This parallels our findings in Malesherbia auristipulata, where specific fungal taxa may associate more closely with particular phenological stages, enhancing the plant’s ability to adapt to extreme conditions. Additionally, recent studies have demonstrated the antagonistic activity of endophytic fungi isolated from medicinal plants such as Ocimum basilicum and Leucas aspera, which inhibit the growth of phytopathogens like Fusarium oxysporum and Aspergillus niger [48]. These findings align with the protective role that endophytic fungi may play in M. auristipulata, helping to maintain plant health and defend against pathogens, which is essential for survival in extreme environments like the Atacama Desert.

3. Materials and Methods

Geographic Location. This study was conducted at Cuesta El Águila, located in the Arica and Parinacota Region of Chile. This site was selected because it is the only known natural habitat where Malesherbia auristipulata forms communities alongside other associated flora species. Cuesta El Águila is part of Quebrada Cardones in the Sierra de Huaylillas (coordinates: S18°28′547″ and W69°51′485″).
Flora Associated with Malesherbia auristipulata. To characterize the plant community of M. auristipulata, samples were collected from all herbaceous and shrub species growing in association with this plant at Cuesta El Águila. A 1000 m transect was surveyed in the lower part of the quebrada, selecting vegetative and reproductive parts of all plants within a 10 m radius around the M. auristipulata specimens under study. All plants were preserved as herbarium specimens and were compared with type species at the National Museum of Natural History for taxonomic identification.
Phenological Study. The monthly and annual phenological study of Malesherbia auristipulata began on 28 January 2019 by tagging 165 specimens, corresponding to the majority of adult plants from the only described community at Cuesta El Águila. Fifteen days later, in February 2019, a strong flash flood severely affected the area, sweeping away 90% of the tagged plants. Due to the population decrease, the study was restarted on 5 March 2019, and 38 adult plants were tagged, including 11 dormant plants, which allowed for the detection of phenophase changes over the course of a year. To increase the sample size, 23 seedlings were included, originating from the germination of seeds forming banks at the base of adult plants (Figure 4). The monthly expeditions allowed for detailed observations of the plants, considering growth, flowering, fruiting, and other phenological events, as well as visits from potential or effective pollinators. A plant was considered to be in flowering or fruiting only if 20% or more of the plant displayed the corresponding phenophase.
Sample Collection for the Study of Endophytic Mycoflora. Samples of seeds, roots, stems, and leaves of M. auristipulata were systematically collected at different times of the year to capture phenological changes and seasonal variability. During each expedition, samples were taken from various organs of different specimens. Only healthy, disease-free plants were selected to ensure a suitable environment for the study of endophytic microorganisms.
The plant samples were washed and disinfected following a strict protocol: first, they were immersed in 95% alcohol for 2 min, followed by 2% sodium hypochlorite for another 2 min, and finally in 70% alcohol for 2 min. Subsequently, the samples were rinsed with sterile distilled water. From this point onward, all procedures were carried out in a laminar flow hood to maintain sterility. The stem samples were cut longitudinally and placed in Petri dishes with specific culture media, such as PDA (potato dextrose agar) and WA (water agar). In the case of roots, the ends and edges were removed, and a piece from the inner zone was placed in the same culture media. The flower and leaf samples were macerated in a porcelain mortar, and the resulting pieces were placed in Petri dishes with PDA (potato dextrose agar) and WA.
Morphological and Molecular Characterization. The endophytic fungi isolated from M. auristipulata were studied both morphologically and molecularly. The macroscopic and microscopic characteristics of the fungal structures were described, and each isolate was cultivated in pure, monospore cultures, recording the macroscopic characteristics of the colonies and the microscopic elements of taxonomic value. From pure cultures, molecular analysis was performed for the precise identification of fungal species.
For this purpose, DNA was extracted from the isolated fungi, and subsequently the internal transcribed spacer region (ITS) was amplified using primers ITS4 (5′-TCCTCCGCTTATTGATATGC-3); and ITS5 (5′-GGAAGTAAAAGTCGTAACAAGG-3′) [49]. The obtained sequences were compared with available databases to determine the taxonomic identity of the species based on sequence similarity.
This combined approach of morphological and molecular characterization allowed for a robust identification of the endophytic fungal species present in Malesherbia auristipulata, providing a more comprehensive understanding of their diversity and potential function in the host plant.

4. Conclusions

The analysis of the plant community of Malesherbia auristipulata in its natural habitat has revealed a diverse plant community well adapted to the extreme conditions of the Atacama Desert. The botanical species that make up this community are native and endemic, with no evidence of introduced species, which is consistent with previous studies on the vegetation of this region [5,20]. The high proportion of endemic species underscores both the uniqueness and fragility of this ecosystem, highlighting the urgent need for its conservation.
The phenology of M. auristipulata and its surrounding plant species provides essential information for understanding seasonal dynamics and ecological interactions in these arid habitats. Phenological records show how extreme climatic events can have drastic effects on the phenology and survival of plants, which in turn impacts the structure and function of the ecosystem [24,29].
The study of endophytic fungi associated with M. auristipulata has revealed a diverse fungal community with significant implications for the plant’s health and adaptation to its environment. The variability in the distribution of these fungi among different parts of the plant suggests complex interactions that may influence the phenology and resilience of M. auristipulata in the face of changing environmental conditions. The presence of endophytic fungi such as Alternaria and Fusarium underscores the importance of these microorganisms in the dynamics of plants in arid ecosystems [15,34].
The study of interactions between phenology, plant community, endophytic fungi, and plant trichomes offers a more comprehensive understanding of the dynamics and health of ecosystems. These interactions not only influence the structure and function of the ecosystem but also the health and performance of the host plants [15,16]. Research in this field is essential for the conservation and sustainable management of natural ecosystems, especially in arid regions where biodiversity and adaptation to extreme conditions are crucial [17,34].
Understanding the dynamics of microorganisms in natural environments and their relationship with host organisms is essential for appreciating microbial diversity and its role in terrestrial ecosystems [35,36]. Microbes, capable of colonizing a wide range of environments—from deserts to poles—demonstrate an adaptability and diversity that underscores their importance in various ecological niches [39], especially in arid ecosystems such as the Atacama Desert [20].

Author Contributions

Conceptualization, G.F.S.C. and E.B.S.; data curation, M.A.M. and W.H.-M.; methodology, E.B.S., W.H.-M., and G.F.S.C.; validation, E.B.S., M.A.M., N.V.S., and G.F.S.C.; formal analysis, G.F.S.C., M.A.M., N.V.S., W.H.-M., and E.B.S.; investigation, E.B.S., M.A.M., W.H.-M., and G.F.S.C.; resources, E.B.S.; writing—original draft preparation, E.B.S., N.V.S., W.H.-M., and G.F.S.C.; writing—review and editing, G.F.S.C., W.H.-M., and N.V.S.; visualization, M.A.M.; supervision, E.B.S.; funding acquisition, G.F.S.C. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by Universidad de Tarapacá, Proyecto Mayor UTA 4728-23.

Data Availability Statement

Data are contained within the article.

Acknowledgments

The authors thank the Dirección de Investigación y Postgrado de la Universidad de Tarapacá for their support in this work.

Conflicts of Interest

The authors declare no conflicts of interest.

References

  1. Garreaud, R.D.; Molina, A.; Farias, M. Andean uplift, ocean cooling and Atacama hyperaridity: A climate modeling perspective. Earth Planet. Sci. Lett. 2010, 292, 39–50. [Google Scholar] [CrossRef]
  2. Seyfried, H.; Wörner, G.; Uhlig, D.; Kohler, I.; Calvo, C. Introducción a la geología y morfología de los Andes en el norte de Chile. Chungará 1999, 30, 7–39. [Google Scholar] [CrossRef]
  3. Eschel, G.; Araus, V.; Undurraga, S.; Soto, D.; Moraga, C.; Montecinos, A.; Moyano, T.; Maldonado, J.; Díaz, F.; Varala, K.; et al. Plant ecological genomics at the limits of life in the Atacama desert. Plant Biol. 2021, 118, e2101177118. [Google Scholar] [CrossRef] [PubMed]
  4. Houston, J.; Hartley, A.J. The central Andean west-slope rainshadow and its potential contribution to the origin of hyper-aridity in the Atacama Desert. Int. J. Clim. 2003, 23, 1453–1464. [Google Scholar] [CrossRef]
  5. Rundel, P.W.; Dillon, M.O.; Palma, B.; Mooney, H.A.; Gulmon, S.L.; Ehleringer, J.R. The Phytogeography and Ecology of the Coastal Atacama and Peruvian Deserts. Aliso A J. Syst. Florist. Bot. 1991, 13, 1–49. [Google Scholar] [CrossRef]
  6. Ruhm, J.; Böhnert, T.; Mutke, J.; Luebert, F.; Montesinos-Tubée, D.B.; Weigend, M. Two Sides of the Same Desert: Floristic Connectivity and Isolation Along the Hyperarid Coast and Precordillera in Peru and Chile. Front. Ecol. Evol. 2022, 10, 1–17. [Google Scholar] [CrossRef]
  7. García, G.M.; Gardeweg, P.M.; Clavero, R.J.; Herail, G. Hoja Arica, Región de Tarapacá; Servicio Nacional de Geología y Minería: Santiago, Chile, 2004; p. 150. [Google Scholar]
  8. Salas, R.; Kast, R.; Montecinos, P.; Salas, I. Geología y Recursos Minerales del Departamento de Arica; Instituto de Investigaciones Geológicas: Santiago, Chile, 1966; p. 111. [Google Scholar]
  9. Arroyo, M.T.K.; Squeo, F.A.; Armesto, J.J.; Villagran, C. Effects of Aridity on Plant Diversity in the Northern Chilean Andes: Results of a Natural Experiment. Ann. Mo. Bot. Gard. 1988, 75, 55. [Google Scholar] [CrossRef]
  10. Morales, M.S.; Crispín-Delacruz, D.B.; Álvarez, C.; Christie, D.A.; Ferrero, E.M.; Andreu-Hayles, L.; Villalba, R.; Guerra, A.; Ticse-Otarola, G.; Rodríguez-Ramírez, E.C.; et al. Drought increase since the mid-20th century in the northern South American Altiplano revealed by a 389-year precipitation record. Clim. Past 2023, 19, 457–476. [Google Scholar] [CrossRef]
  11. Veloso, J.M.V. Analysis of an extreme precipitation event in the Atacama Desert on January 2020 and its relationship to humidity advection along the Southeast Pacific. Atmosfera 2020, 35, 421–448. [Google Scholar] [CrossRef]
  12. Benoit, C. Libro Rojo de La Flora Terrestre de Chile, (Primera Parte); Corporación Nacional Forestal: Santiago, Chile, 1989; p. 157. [Google Scholar]
  13. Ministerio del Medio Ambiente. Aprueba y oficializa clasificación de especies según estado de conservación, Décimosexto Proceso; Diario Oficial de la República de Chile, Ministerio del Interior y Seguridad Pública: Santiago, Chile, 2020; pp. 1–6. [Google Scholar]
  14. Carevic, F.S.; Delatorre-Herrera, J.; Carrasco, A. Plant water variables and reproductive traits are influenced by seasonal climatic variables in Prosopis burkartii (Fabaceae) at Northern Chile. Flora Morphol. Distrib. Funct. Ecol. 2017, 233, 7–11. [Google Scholar] [CrossRef]
  15. Baron, N.C.; Rigobelo, E.C. Endophytic fungi: A tool for plant growth promotion and sustainable agriculture. Mycology 2022, 13, 39–55. [Google Scholar] [CrossRef] [PubMed]
  16. Rodríguez, R.J.; White, J.F.; Arnold, A.E.; Redman, R.S. Fungal endophytes: Diversity and functional roles: Tansley review. N. Phytol. 2009, 182, 314–330. [Google Scholar] [CrossRef] [PubMed]
  17. Redman, R.S.; Sheehan, K.B.; Stout, R.G.; Rodriguez, R.J.; Henson, J.M. Thermotolerance Generated by Plant/Fungal Symbiosis. Science 2002, 298, 1581. [Google Scholar] [CrossRef] [PubMed]
  18. Herre, E.A.; Mejía, L.C.; Mejía, M.; Kyllo, D.A.; Rojas, E.; Maynard, Z.; Butler, A.; Van Bael, S.A. Ecological implications of anti-pathogen effects of tropical fungal endophytes and mycorrhizae. Ecology 2007, 88, 550–558. [Google Scholar] [CrossRef] [PubMed]
  19. Rodríguez, R.; Marticorena, C. Catálogo de Las Plantas Vasculares de Chile; Editorial Universidad de Concepción: Santiago, Chile, 2019; p. 424. [Google Scholar]
  20. Pinto, R.; Luebert, F. Data on the vascular flora of the coastal desert of Arica and Tarapacá, Chile, and its phytogeographical relationships with southern Perú. Gayana Bot. 2009, 66, 28–49. [Google Scholar]
  21. Camacho, C.; Coulouris, G.; Avagyan, V.; Ma, N.; Papadopoulos, J.; Bealer, K.; Madden, T.L. BLAST+: Architecture and applications. BMC Bioinform. 2009, 10, 421. [Google Scholar] [CrossRef]
  22. Innis, M.A.; Gelfand, D. Optimization of PCRs. In PCR Protocols: A Guide to Methods and Applications; Academic Press: San Diego, CA, USA, 1990; pp. 3–12. [Google Scholar]
  23. Khalmuratova, I.; Choi, D.-H.; Woo, J.-R.; Jeong, M.-J.; Oh, Y.; Kim, Y.-G.; Lee, I.-J.; Choo, Y.-S.; Kim, J.-G. Diversity and Plant Growth-Promoting Effects of Fungal Endophytes Isolated from Salt-Tolerant Plants. J. Microbiol. Biotechnol. 2020, 30, 1680–1687. [Google Scholar] [CrossRef]
  24. Rathcke, B.; Lacey, E.P. Phenological Patterns of Terrestrial Plants. Annu. Rev. Ecol. Syst. 1985, 16, 179–214. [Google Scholar] [CrossRef]
  25. Arroyo, M.T.K.; Armesto, J.J.; Villagran, C. Plant Phenological Patterns in the High Andean Cordillera of Central Chile. J. Ecol. 1981, 69, 205–223. [Google Scholar] [CrossRef]
  26. Tilman, D. Resource Competition and Community Structure; Princeton University Press: Oxford, UK, 1982; p. 294. [Google Scholar]
  27. Arnold, A.E.; Mejía, L.C.; Kyllo, D.; Rojas, E.I.; Maynard, Z.; Robbins, N.; Herre, E.A. Fungal endophytes limit pathogen damage in a tropical tree. Proc. Natl. Acad. Sci. USA 2003, 100, 15649–15654. [Google Scholar] [CrossRef]
  28. Clay, K. Fungal Endophytes of Grasses: A Defensive Mutualism between Plants and Fungi. Ecology 1988, 69, 10–16. [Google Scholar] [CrossRef]
  29. Holmgren, M.; Stapp, P.; Dickman, C.R.; Gracia, C.; Graham, S.; Gutiérrez, J.R.; Hice, C.; Jaksic, F.; Kelt, D.A.; Letnic, M.; et al. Extreme climatic events shape arid and semiarid ecosystems. Front. Ecol. Environ. 2006, 4, 87–95. [Google Scholar] [CrossRef]
  30. Akram, S.; Ahmed, A.; He, P.; He, P.; Liu, Y.; Wu, Y.; Munir, S.; He, Y. Uniting the Role of Endophytic Fungi against Plant Pathogens and Their Interaction. J. Fungi 2023, 9, 72. [Google Scholar] [CrossRef] [PubMed]
  31. Porras-Alfaro, A.; Bayman, P. Hidden Fungi, Emergent Properties: Endophytes and Microbiomes. Annu. Rev. Phytopathol. 2011, 49, 291–315. [Google Scholar] [CrossRef]
  32. García-Orenes, F.; Guerrero, C.; Roldán, A.; Mataix-Solera, J.; Cerdà, A.; Campoy, M.; Zornoza, R.; Bárcenas, G.; Caravaca, F. Soil microbial biomass and activity under different agricultural management systems in a semiarid Mediterranean agroecosystem. Soil Tillage Res. 2010, 109, 110–115. [Google Scholar] [CrossRef]
  33. Gorbushina, A.A. Life on the rocks. Environ. Microbiol. 2007, 9, 1613–1631. [Google Scholar] [CrossRef]
  34. Rothschild, L.J.; Mancinelli, R.L. Life in extreme environments. Nature 2001, 409, 1092–1101. [Google Scholar] [CrossRef]
  35. Pointing, S.B.; Belnap, J. Microbial colonization and controls in dryland systems. Nat. Rev. Microbiol. 2012, 10, 551–562. [Google Scholar] [CrossRef]
  36. Lindow, S.E.; Brandl, M.T. Microbiology of the Phyllosphere. Appl. Environ. Microbiol. 2003, 69, 1875–1883. [Google Scholar] [CrossRef]
  37. Levin, D.A. The Role of Trichomes in Plant Defense. Q. Rev. Biol. 1973, 48, 3–15. [Google Scholar] [CrossRef]
  38. Wagner, G.J. Secreting Glandular Trichomes: More than Just Hairs. Plant Physiol. 1991, 96, 675–679. [Google Scholar] [CrossRef] [PubMed]
  39. Leveau, J.H. Microbial communities in the phyllosphere. In Biology of the Plant Cuticle; Riederer, M., Müller, C., Eds.; Blackwell Publishing: Hoboken, NJ, USA, 2006; pp. 334–359. [Google Scholar]
  40. Kabir, N.; Wahid, S.; Rehman, S.U.; Qanmber, G. The intricate world of trichome development: From signaling pathways to transcriptional regulation. Environ. Exp. Bot. 2024, 217, 105549. [Google Scholar] [CrossRef]
  41. Karabourniotis, G.; Liakopoulos, G.; Nikolopoulos, D.; Bresta, P. Protective and defensive roles of non-glandular trichomes against multiple stresses: Structure–function coordination. J. For. Res. 2020, 31, 1–12. [Google Scholar] [CrossRef]
  42. Yamada, M.; Sonoda, R. A Fluorescens microscopic study of the infection process of Discula theae-sinensis in tea. JARQ 2014, 48, 399–402. [Google Scholar] [CrossRef]
  43. Niremberg, H.; O’Donnell, K. New Fusarium species and combinations within the Giberella fujikuroi species complex. Mycologia 1998, 3, 434–438. [Google Scholar] [CrossRef]
  44. Elvira-Recuenco, M.; Iturritxa, E.; Majada, J.; Alia, R.; Raposo, R. Adaptive potential of maritime pine (Pinus pisaster) populations to the emerging pitck canker pathogen, Fusarium circinatum. PLoS ONE 2014, 12, e114971. [Google Scholar]
  45. Hernandez-Escribano, L.; Visser, E.A.; Iturritxa, E.; Raposo, R.; Naidoo, S. The transcriptome of Pinus pinaster under Fusarium circinatum challenge. BMC Genom. 2020, 21, 28–36. [Google Scholar] [CrossRef]
  46. Maria, Z.; Shamsi, S.; Hosen, S.; Bashar, A. Morpho-Molecular Characterization of Endophytic Fungi from Three Traditional Medicinal Plants. Bangladesh J. Bot. 2024, 53, 361–372. [Google Scholar] [CrossRef]
  47. Lin, X.-R.; Yang, D.; Wei, Y.-F.; Ding, D.-C.; Ou, H.-P.; Yang, S.-D. Amaranth Plants with Various Color Phenotypes Recruit Different Soil Microorganisms in the Rhizosphere. Plants 2024, 13, 2200. [Google Scholar] [CrossRef]
  48. Devi, W.; Surendirakumar, K. In vitro antagonistic activity of endophytic fungi associated with medicinal plants of Lamiaceae towards phytopathogenic fungi. J. Mycopathol. Res. 2024, 62, 447–451. [Google Scholar]
  49. White, T.J.; Bruns, T.D.; Lee, S.B.; Taylor, J.W. Amplification and Direct Sequencing of Fungal Ribosomal RNA Genes for Phylogenetics. In PCR Protocols: A Guide to Methods and Applications; Innis, M.A., Gelfand, D.H., Sninsky, J.J., White, T.J., Eds.; Academic Press: New York, NY, USA, 1990; pp. 315–322. [Google Scholar]
Plants 13 03035 g001
Figure 1. Malesherbia auristipulata in its natural habitat, Cuesta El Águila, Quebrada Cardones, Arica and Parinacota Region: (A) adult plant, (B) flower, (C) vegetative buds, (D) glandular trichomes on leaves, and (E) seeds.
Figure 1. Malesherbia auristipulata in its natural habitat, Cuesta El Águila, Quebrada Cardones, Arica and Parinacota Region: (A) adult plant, (B) flower, (C) vegetative buds, (D) glandular trichomes on leaves, and (E) seeds.
Plants 13 03035 g001
Plants 13 03035 g002
Figure 2. Abundance (number of individuals) recorded at 49 sampling points along a 20 m transect, Cuesta El Águila, Quebrada de Cardones, Arica and Parinacota Region.
Figure 2. Abundance (number of individuals) recorded at 49 sampling points along a 20 m transect, Cuesta El Águila, Quebrada de Cardones, Arica and Parinacota Region.
Plants 13 03035 g002
Plants 13 03035 g003
Figure 3. Plant species that are part of the plant community of Malesherbia auristipulata: (A) Solanum peruvianum, (B) Glandularia gynobasis, (C) Senecio zapahuirensis, (D) Nolana rhombifolia, (E) Allionia incarnata, (F) Hoffmannseggia minor, (G) Cistanthe sp., and (H) Spergularia fasciculata.
Figure 3. Plant species that are part of the plant community of Malesherbia auristipulata: (A) Solanum peruvianum, (B) Glandularia gynobasis, (C) Senecio zapahuirensis, (D) Nolana rhombifolia, (E) Allionia incarnata, (F) Hoffmannseggia minor, (G) Cistanthe sp., and (H) Spergularia fasciculata.
Plants 13 03035 g003
Plants 13 03035 g004
Figure 4. Stacked area charts representing the phenological behavior of Malesherbia auristipulata throughout the year, comparing the growth phases between juvenile and adult plants in percentage terms. The charts are divided into four phenological categories: vegetative, flowering, fruiting, and dormancy.
Figure 4. Stacked area charts representing the phenological behavior of Malesherbia auristipulata throughout the year, comparing the growth phases between juvenile and adult plants in percentage terms. The charts are divided into four phenological categories: vegetative, flowering, fruiting, and dormancy.
Plants 13 03035 g004
Plants 13 03035 g005
Figure 5. Colonies of endophytic fungi on APD medium, isolated from Malesherbia auristipulata. A9: Alternaria alstroemeriae NR_163686.1, A23: A. alstroemeriae NR_163686.1, A7: A. sorghi NR_160246.1, A39: A. sorghi NR_160246.1, A59: Aureobasidium melanogenum NR_159598.1, A37: Didymella keratinophila NR_158275.1, A19: Fusarium biomiforme NR_111885.1, A14: F. circinatum NR_120263.1, A13: F. nurragi NR_159860.1, and A58: F. nurragi NR_159860.1.
Figure 5. Colonies of endophytic fungi on APD medium, isolated from Malesherbia auristipulata. A9: Alternaria alstroemeriae NR_163686.1, A23: A. alstroemeriae NR_163686.1, A7: A. sorghi NR_160246.1, A39: A. sorghi NR_160246.1, A59: Aureobasidium melanogenum NR_159598.1, A37: Didymella keratinophila NR_158275.1, A19: Fusarium biomiforme NR_111885.1, A14: F. circinatum NR_120263.1, A13: F. nurragi NR_159860.1, and A58: F. nurragi NR_159860.1.
Plants 13 03035 g005
Table 1. Plant community of Malesherbia auristipulata in Cuesta El Águila, Quebrada Cardones, Arica and Parinacota Region, Chile.
Table 1. Plant community of Malesherbia auristipulata in Cuesta El Águila, Quebrada Cardones, Arica and Parinacota Region, Chile.
FamilyScientific NameCommon NameNative/EndemicHabitDistribution *
AizoaceaeTetragonia microcarpa Phil.Aguanosanativeannual herbAYP, TAR, ANT, ATA
AsteraceaeAmbrosia artemisioides Meyen & Walp. ex MeyenTikara, Pikara, Cadillo, Chaspaksa, Monte verde, Tola negra, Pegapega, LipelipenativeshrubAYP, TAR, ANT
AsteraceaeSenecio zapahuirensis Martic. & QuezadaDesconocidoendemicshrubAYP, TAR
AsteraceaeTrichocline caulescens Phil.Wanti, Garra de león, Bailabailaendemicperennial herbAYP, TAR, ANT
AsteraceaeTrixis cacalioides (Kunth) D. DonVisavisanativeshrubAYP, TAR, ANT, ATA
ChenopodiaceaeAtriplex glaucescens Phil.Juirajuira, PiyayaendemicshrubAYP, TAR, ANT, ATA
ChenopodiaceaeChenopodium petiolare Kunth.Juirajuira, Kañawa, Quinua de gentiles, Piyaya hembranativeperennial herbAYP, TAR, ANT, ATA, COQ, VAL
FabaceaeHoffmannseggia minor (Phil.) UlibarriAlgarrobilla, Bilankichu, Kulchau, Mutukuru, Motokoronativeperennial herbAYP, TAR, ANT
MalvaceaeCristaria dissecta Hook. & Arn. var. DissectaMalvavisco, Malvanativeperennial herbAYP, TAR, ANT, ATA, COQ, VAL, RME, LBO
MalvaceaeTarasa operculata (Cav.) Krapov.Poq’ot’ola, Qhella hembra, Qhella blanca, Malva, TarasanativeshrubAYP, TAR, ANT
MontiaceaeCistanthe amarantoides (Phil.) Carolin ex HerschkovitzAnojarjinchu, Tiqintiqi, Oreja de chanchoendemicperennial herbAYP, TAR, ANT, ATA, COQ
NycataginaceaeAllionia incarnata L. (hierba perenne, nativa)Desconocidonativeperennial herbAYP, TAR, ANT, ATA
PassifloraceaeMalesherbia auristipulata RicardiAjí de zorra, PiojilloendemicshrubAYP, TAR
SolanaceaeExodeconus flavus (I.M. Johnst.) Axelius & D’ArcyDesconocidonativeannual herbAYP, TAR
SolanaceaeNolana rhombifolia Martic. & QuezadaSuspiroendemicannual herbAYP
SolanaceaeReyesia juniperoides (Werderm.) D’ArcyCanchalahuaendemicperennial herbAYP, TAR
SolanaceaeSolanum peruvianum L.Tomatillonativeperennial herbAYP, TAR
VerbenaceaeGlandularia gynobasis (Wedd.) N. O’Leary & P. PeraltaNametusangaya, Mamapasankayo, Flor del campoendemicperennial herbAYP, TAR
*: Distribution in Chile: The abbreviations used in the table correspond to the country’s political–administrative divisions: AYP (Arica and Parinacota), TAR (Tarapacá), ANT (Antofagasta), ATA (Atacama), COQ (Coquimbo), VAL (Valparaíso), RME (Metropolitan Region of Santiago), and LBO (Libertador General Bernardo O’Higgins).
Table 2. Annual phenology of adult and juvenile Malesherbia auristipulata plants in Cuesta El Águila, Quebrada Cardones, Arica and Parinacota Region. The numbers represent the percentage of individuals in each phenophase.
Table 2. Annual phenology of adult and juvenile Malesherbia auristipulata plants in Cuesta El Águila, Quebrada Cardones, Arica and Parinacota Region. The numbers represent the percentage of individuals in each phenophase.
Vegetative (%)Flowering (%)Fruiting (%)Dead (%)
Month/PhenophaseAdultJuvenileAdultJuvenileAdultJuvenileAdultJuvenile
Jan.81.610015.802.6000
Feb.81.610015.802.6000
Mar.73.710021.105.3000
Apr.68.410023.707.9000
May63.210028.907.9000
Jun.65.895.726.34.37.9000
Jul.57.982.628.94.313.28.704.3
Aug.57.973.926.38.715.88.708.7
Sep.57.986.936.805.34.408.7
Oct.61.178.325.04.313.90117.4
Nov.61.869.617.6020.60230.4
Dec.62.956.517.14.3200239.2
Table 3. Diversity of endophytic fungi associated with Malesherbia auristipulata.
Table 3. Diversity of endophytic fungi associated with Malesherbia auristipulata.
CodeBLASTN Identity% IdentityRootStemLeaf
A9Alternaria alstroemeriae NR_163686.199.82+
A23Alternaria alstroemeriae NR_163686.1100+
A7Alternaria sorghi NR_160246.199.83+
A17Alternaria sorghi NR_160246.199.83 +
A30Alternaria sorghi NR_160246.199.65+
A34Alternaria sorghi NR_160246.199.13 +
A36Alternaria sorghi NR_160246.199.65 +
A39Alternaria sorghi NR_160246.199.65 +
A44Alternaria sorghi NR_160246.199.83+
A55Alternaria sorghi NR_160246.199.65 +
A61Alternaria sorghi NR_160246.199.65 +
A62Alternaria sorghi NR_160246.199.83 +
A63Alternaria sorghi NR_160246.199.83 +
A59Aureobasidium melanogenum NR_159598.199.49 +
A37Didymella keratinophila NR_158275.199.82 +
A19Fusarium biomiforme NR_111885.184.83+
A14Fusarium circinatum NR_120263.197.85 +
A13Fusarium nurragi NR_159860.192.93 +
A58Fusarium nurragi NR_159860.191.96+
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

Sepúlveda Chavera, G.F.; Belmonte Schwarzbaum, E.; Valderrama Saez, N.; Arismendi Macuer, M.; Huanca-Mamani, W. Phenological and Fungal Interactions of Malesherbia auristipulata Ricardi (Passifloraceae) in the Atacama Desert: Adaptations and Conservation in an Extreme Ecosystem. Plants 2024, 13, 3035. https://doi.org/10.3390/plants13213035

AMA Style

Sepúlveda Chavera GF, Belmonte Schwarzbaum E, Valderrama Saez N, Arismendi Macuer M, Huanca-Mamani W. Phenological and Fungal Interactions of Malesherbia auristipulata Ricardi (Passifloraceae) in the Atacama Desert: Adaptations and Conservation in an Extreme Ecosystem. Plants. 2024; 13(21):3035. https://doi.org/10.3390/plants13213035

Chicago/Turabian Style

Sepúlveda Chavera, German F., Eliana Belmonte Schwarzbaum, Nicolas Valderrama Saez, Mabel Arismendi Macuer, and Wilson Huanca-Mamani. 2024. "Phenological and Fungal Interactions of Malesherbia auristipulata Ricardi (Passifloraceae) in the Atacama Desert: Adaptations and Conservation in an Extreme Ecosystem" Plants 13, no. 21: 3035. https://doi.org/10.3390/plants13213035

APA Style

Sepúlveda Chavera, G. F., Belmonte Schwarzbaum, E., Valderrama Saez, N., Arismendi Macuer, M., & Huanca-Mamani, W. (2024). Phenological and Fungal Interactions of Malesherbia auristipulata Ricardi (Passifloraceae) in the Atacama Desert: Adaptations and Conservation in an Extreme Ecosystem. Plants, 13(21), 3035. https://doi.org/10.3390/plants13213035

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