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Review

Trichoderma Diversity in Mexico: A Systematic Review and Meta-Analysis

by
Hector Osvaldo Ahedo-Quero
1,
Teodulfo Aquino-Bolaños
1,*,
Yolanda Donají Ortiz-Hernández
1,* and
Edgar García-Sánchez
2
1
Instituto Politécnico Nacional, CIIDIR-Oaxaca, Hornos 1003, Santa Cruz Xoxocotlán, Oaxaca 71230, Mexico
2
CONAHCYT-Instituto Politécnico Nacional, Centro Interdisciplinario de Investigación para el Desarrollo Integral Regional Unidad Oaxaca, Hornos 1003, Santa Cruz Xoxocotlán, Oaxaca 71230, Mexico
*
Authors to whom correspondence should be addressed.
Diversity 2024, 16(1), 68; https://doi.org/10.3390/d16010068
Submission received: 7 November 2023 / Revised: 17 January 2024 / Accepted: 17 January 2024 / Published: 20 January 2024
(This article belongs to the Special Issue Biodiversity and Ecology of Soil Fungal Communities)
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Abstract

:
Trichoderma is a genus of cosmopolitan fungi with more than 375 species described today. Despite its global significance in agriculture, ecosystems, and industry, few studies have focused on studying the diversity and distribution of this genus in Mexico. In this systematic review and meta-analysis, we aimed to understand the diversity and distribution of Trichoderma species in Mexico, both in ecosystems and agroecosystems. For this systematic review, we used the PRISMA methodology. We reviewed forty-one scientific articles, two book chapters, and the GBIF database. We recorded a total of 1082 isolates, revealing the presence of 57 species of the genus Trichoderma in 29 states of Mexico. We found that species from the genus Trichoderma were reported in 20 agroecosystems and 6 ecosystems. T. harzianum was the predominant species in both agricultural and undisturbed soil. Tabasco and Veracruz were the states with the highest species diversity, with 20 and 14 species reported, respectively. Chiapas had the highest diversity indices (Menhinick had 3.20, Simpson had 0.89, and Margalef had 4.16). The coffee crop was the agroecosystem with the highest diversity, with 12 species reported. In the undisturbed ecosystems, tropical rainforests featured 12 different species. This study highlights the distribution of the genus Trichoderma as a cosmopolitan genus. We argue for the importance of the species that comprise the genus and its applications for social benefits.

1. Introduction

Trichoderma is a genus that belongs to the Fungi Kingdom, Ascomycota Division, Pezizomycotina Subdivision, Sordariomycetes Class, Hypocreales Order, and Hypocraceae Family. Globally, 375 species have been described and validated [1]. Species of this genus exhibit a cosmopolitan distribution, inhabiting various ecosystems and substrates, including agricultural fields, grasslands, swamps, forests, marshes, deserts, and water bodies [2,3].
The Trichoderma species play crucial roles in ecosystems and agroecosystems by controlling plant pests and diseases, acting as a biofertilizer, degrading organic matter, and participating in multitrophic interactions along with insects [4,5,6]. Therefore, researchers have been exploring ways to harness the properties of Trichoderma species for their application in agriculture, industry, and environmental bioremediation.
In Mexico, studies addressing this fungi genus have focused on its efficacy as a biological control agent against diseases in crops such as agave (Agave tequilana), avocado (Persea americana), garlic (Allium sativum), lettuce (Lactuca sativa), peanuts (Arachis hypogaea), cocoa (Theobroma cacao), coffee (Coffea arabica), cinnamon (Cinnamomum verum), onion (Allium cepa), chili (Capsicum annuum), hibiscus (Hibiscus sabdariffa), corn (Zea mays), beans (Phaseolus vulgare), apples (Malus domestica), mango (Mangifera indica), walnuts (Juglans regia) and bananas (Musa × paradisiaca) [7,8,9,10,11,12,13,14,15,16,17,18,19,20,21,22].
In the industrial context, Hernández-Melchor et al. (2019) [23] underscored the importance of Trichoderma during the process of biofuel production. Biofuels are produced through the secretion of enzymes and the production of secondary metabolites of the Trichoderma species. On an environmental front, Trichoderma has demonstrated its capability to degrade polycyclic aromatic hydrocarbons in soil contaminated with crude oil [24]. Consequently, a study on the biodiversity and distribution of species of the genus Trichoderma is paramount, offering crucial insights into the potential of native species and their application in biotechnology.
Studies addressing the diversity and distribution of the genus Trichoderma are scarce in Mexico. One approach to address the lack of information on this genus is through a systematic review that provides reliable and accurate information. Utilizing contextual data and gene sequences accessible through digital databases enables the acquisition and generation of novel knowledge [25]. In this study, we conducted a systematic review to comprehensively address the knowledge gaps and furnish dependable insights into the diversity and distribution of Trichoderma species.
In a meta-analysis, ensuring transparency, completeness, and accuracy is essential for the reproducibility of these analyses and for promoting valid cross-comparisons among studies. In this context, the PRISMA methodology (Reference Elements for Publishing Systematic Reviews and Meta-Analyses) functions as a valuable tool that standardizes systematic reviews and facilitates the collection of reproducible information [26]. Thus, when using the PRISMA methodology, we can obtain data on the abundance and presence of Trichoderma species, the number of species, geographical locations, dates, and other data that allow us to conduct ecological analyses. While ecological information is often overlooked in the study of microorganisms, it holds significant value. Ecological studies can provide valuable insights to generate novel study approaches and applications for microorganisms such as the fungi of the genus Trichoderma [27].
The limited number of studies on the genus Trichoderma available in Mexico cover various areas of knowledge. Thus, we can obtain information that generates more analysis and new studies on the ecology and diversity of this genus. Some studies on the diversity of the genus Trichoderma in Mexico focus on calculating indices based on the quantification of the number of present species. Examples of such studies are those conducted by Sánchez & Rebolledo (2010) [22], Torres-De la Cruz et al. (2015) [28], and Sánchez Hernández et al. (2018) [29], who calculated Margalef indices for this genus, obtaining values of 0.71 (in Agave tequilana), 1.75, and 2.48 (in Theobroma cacao), respectively.
To date, no systematic review with meta-analysis has been conducted to analyze the diversity and distribution of species of the genus Trichoderma in Mexico. This paper aims to fill this knowledge gap by providing a systematic review and meta-analysis to understand the biodiversity and distribution of this genus in Mexico.
This is the first attempt to understand the diversity of the genus Trichoderma and its distribution in Mexico, providing a reference regarding the ecological aspects of the genus Trichoderma for future research.

2. Materials and Methods

We conducted a systematic review and meta-analysis using the PRISMA (Preferred Reporting Items for Systematic Reviews and Meta-Analyses) methodology [26].

2.1. Study Area

We searched the primary literature, which encompassed studies conducted in Mexico.

2.2. Searching for Information

We conducted a search using the following electronic databases: Scopus, Springer, BioOne, Web of Science, Google Scholar, Pubmed, and Science Direct, as well as the Global Biodiversity Information Facility (GBIF, https://www.gbif.org/es/ accessed on 16 November 2021) platform. Our search spanned articles, reviews, and book chapters, along with georeferenced records of fungal species belonging to the genus Trichoderma (GBIF platform). Grey unpublished literature was not used for the analyses.
To conduct our search, we used the following search terms: “fungal diversity”, “fungal biodiversity”, “Trichoderma”, “Trichoderma biodiversity”, “ascomycetes biodiversity”, “ascomycetes”, “micromycetes”, “soil microbiology”, “Hypocreales”. We combined the above terms with the words “Mexico” and with the names of each of its states. To broaden our search, we used Boolean operators (AND, OR, NOT) to combine the search terms. The search period extended from January 2000 to January 2022.

2.3. Eligibility Criteria in Published Articles

Articles that met the following criteria were included in the review and meta-analysis:
  • Research articles and book chapters in English and Spanish in which the isolation and identification of native strains belonging to the genus Trichoderma within the Mexican territory was mentioned.
  • Articles in which the identification of the fungus was conducted at the species level, either morphologically, molecularly, or both.
  • Articles that presented a description of the sampling area where the species was recorded by mentioning the locality, geographical coordinates, or other georeferencing parameters.
  • Articles that featured the use of commercial species were discarded.
  • We also discarded articles that reported repeated strains of species for the same sampling site.
The process of document acquisition is explained in Figure 1.

2.4. Eligibility Criteria for Data on the GBIF Platform

  • We included records where the fungus strains were identified at the species levels.
  • We included records that provided information about the sampling site or the georeferenced location where the strains were isolated.
  • Records from the platform that were repeated in any other document found from other databases were discarded.

2.5. Data Extraction and Conditioning Process

We systematically extracted the following information from the documents: (1) the document type (article, book chapter, or review), (2) document title, (3) author’s name, (4) publication year, (5) state, (6) municipality, (7) the substrate or crop in which the strain was isolated, (8) identification type (morphological, molecular or both), (9) access code to the Digital Database of Genetic Sequences (GENBANK) for species identified molecularly, (10) the identifier assigned by the author to the species in the article. To ensure accuracy, we cross-validated the species’ reported names using the International Commission on the Taxonomy of Trichoderma website (https://trichoderma.info/ accessed on 1 November 2021) in order to use currently valid names for this review.
For the records obtained from the GBIF database, we included strains identified at the species level that provided geographical information. To prevent duplicates, we also looked on the internet for the authors who studied this species to investigate whether data had already been published in a scientific article or other type of document.

2.6. Data Analysis

We conducted the following two types of analyses: (1) qualitative (a descriptive summary) and (2) quantitative (the correlation analysis, a biodiversity permutation test, calculation of diversity indices, and calculation of Bray–Curtis similarity indices).
For the quantitative analyses, we calculated the correlations between the following variables: Year, N° of articles, species, N° of isolates. We conducted a biodiversity permutation test using abundance and species diversity by source of information (GBIF and Systematic review). For the calculation of diversity indices, and calculation of Bray-Curtis similarity indices, we built a matrix with the variables, abundance, sampling site (states), and vegetation type in which the strain was recorded. We processed these data in the statistical program “Paleontological Statistics for Education and Data Analysis version 4.0” (PAST) [30]. We calculated diversity indices separately for the systematic review (SR) and for the GBIF database. We also ran the analyses, including both sources of information (SR + GBIF), in the same analysis. For a more nuanced understanding, we computed Diversity indices and Bray–Curtis similarity indices for the crops and non-disturbed areas separately.

3. Result

3.1. Qualitative Analysis

In the systematic review (SR), the search was extended across 29 scientific journals. We included in the review a total of 41 scientific articles and two book chapters that met the inclusion criteria (Table S1). To enhance organization, we categorized articles and book chapters by the following areas of knowledge: biofuels, ecology, biofertilization, biological control, biological control and biofertilization, and bioremediation (Figure 2).
In terms of publication year, our findings indicate that in 2001, only one published article authored by Michel-Aceves et al., 2001 [31] was identified. Notably, 2020 was the year with the highest number of published articles, with a total of six published articles focused on some aspect of Trichoderma (Figure 3).
Most of the articles found were published in the Mexican Journal of Phytopathology and the Mexican Journal of Mycology, with 6 and 4 articles, respectively (Table 1).
Our findings indicate that species from the genus Trichoderma were reported in 25 states of Mexico (871 isolates representing 38 species). We found that the state of Guerrero contributed the highest number of articles (7 articles reporting 7 species), while the state of Tabasco contributed the highest number of isolates (318 isolates reporting 17 species) (See Table 2).
We found that the GBIF database (Table S2) reports species of Trichoderma in 20 Mexican states, with 207 isolates and 38 species (the species reported in GBIF may differ from those found in electronic journals). According to the GBIF database, Michoacán had the highest number of isolates (57), while Durango had the highest number of species (13).
Combining data from the systematic review (electronic journals) and the GBIF database, we found that species of Trichoderma were reported in 29 of the 32 Mexican states, with 1082 isolates and a diversity of 57 species (Table 2).
When analyzing the results at the species level, Trichoderma harzianum stands out as the most frequently reported species. In this systematic review, the species appears in 161 isolates. By contrast, the GBIF platform’s data show 49 isolates of T. harzianum. When combining data from the systematic review (electronic journals) and the GBIF platform, we found 210 T. harzianum isolates (Figure 4).
In our systematic review (electronic journals), Tabasco had the highest diversity of Trichoderma species (17 species). Based on the information obtained from the GBIF platform, Durango appears as the state with the greatest species diversity (13 species). However, when we merged data from both the systematic review and GBIF, Tabasco appeared as the state with the highest diversity and number of isolates (20 species and 335 isolates, respectively) (Figure 5 and Figure 6).
In our systematic review, we reported different Trichoderma species in agricultural and disturbed soil. The crops associated with these types of soil included the following 20 species: agave (Agave tequilana), avocado (Persea americana), garlic (Allium sativum), lettuce (Lactuca sativa), peanuts (Arachis hypogaea), cocoa (Theobroma cacao L.), coffee (Coffea arabica), cinnamon (Cinnamomum verum), onion (Allium cepa), chili (Capsicum annuum), sunflower (Helianthus annuus), hibiscus (Hibiscus sabdariffa), corn (Zea mays), beans (Phaseolus vulgare), apples (Malus domestica), mango (Mangifera indica), walnuts (Juglans regia), bananas (Musa × paradisiaca), sorghum (Sorghum spp.) and wheat (Triticum spp.). Coffee appeared as the crop with the highest associated species diversity (13 species). Trichoderma harzianum appeared as the most abundant species in agricultural soil. This species appeared in 14 of the 20 reported crops (Figure 7).
The undisturbed soil reported in our review included soil from the mountain mesophyll forest, temperate forest, xerophytic scrub, tropical rainforest, tropical semideciduous forest, and mountain cloud forest. We found that the most common Trichoderma species reported in undisturbed soil was T. harzianum, occurring in four soil types. We also found that the tropical rainforests were reported to have the highest species diversity (12 species reported). In total, 16 species of Trichoderma were reported in undisturbed soil (Figure 8).

3.2. Quantitative Analysis

We found a positive correlation (R = 0.58) between the number of articles and the year of publication, indicating a linear increment in the number of publications over time. We found a strong correlation between the number of isolates and the number of species reported in the systematic review (R = 0.76).
The results of the diversity permutation test show no statistically significant difference between the species diversity found using our search in electronic journals (systematic review) and the GBIF platform.
An analysis of diversity indices based on the systematic review data showed that Tabasco had the highest diversity indices (Shannon index: 2.54; Margalef index: 2.94; Figure 9).
Using the data from GBIF, we found that Chiapas had the highest biodiversity indices (Shannon index: 2.753; Margalef index: 3.909; Menhinick index: 3.20; Figure 10).
Using the data obtained from electronic journals (in the systematic review) combined with the data obtained from GBIF, we found that Chiapas had the highest diversity indices (Margalef index: 4.16; Shannon index: 2.80; and Menhinick index: 3.20; Figure 11).
The results of the Bray–Curtis index analysis showed two distinct groups with no shared similarities. The first group was unique to the state of Morelos, characterized by the exclusive presence of species such as Trichoderma crassum, T. atrobrunneum, T. koreanum, T. pleuroti, and T. pubescens. Within these species, T. crassum was the only species shared with other states. The second group included all the remaining states, which were further divided into two subgroups. The first of these subgroups contained Tabasco and Veracruz (Bray–Curtis index: 0.22). The remaining states collectively formed the second subgroup (Figure 12).
The analysis of crop diversity indices revealed that coffee crops (Coffea arabica) exhibited the highest values for the Simpson index (0.80) and the Shannon index (1.95). By contrast, mango crops (Mangifera indica) stood as the crops showing the highest Margalef index (2.33), while banana crops (Musa × paradisiaca) showed the highest Menhinick index value (1.87) (Figure 13).
We also found that the crops of sunflower (Helianthus annuus), cinnamon (Cinnamomum verum), and chili (Capsicum annuum) showed lower similarity compared to the second group comprising other crops (Figure 14).
Regarding the undisturbed areas, the rainforest had the highest diversity values considering the Simpson (0.8979), Shannon (2.366), and Margalef (2.607) indices. Temperate forests and the Xerophilus scrub showed higher diversity values considering the Menhinick index (Figure 15).
The Bray–Curtis analysis identified two distinct groups. The first group, associated with the tropical semideciduous forest, showed no similarities with the second group. In contrast, the second group showed more resemblance among its members (Figure 16).

4. Discussion

This study represents the first systematic review of aspects of the Trichoderma genus in Mexico. The results revealed a significant diversity of species, with 57 species identified in Mexico. Given the global count of 375 species registered [1], this is a noteworthy contribution, implying that 15.2% of the global Trichoderma species diversity is currently registered in Mexico. Therefore, it is essential to continue exploring and sampling to better understand the diversity of the species of Trichoderma in this country.
Notably, 22 articles in our review were focused on biological control, underscoring the importance and effectiveness of using native Trichoderma species for controlling plant diseases [61]. This trend aligns with other findings from China, where native species have also been used for biological control applications [62].
Further, this work reports a total of 57 Trichoderma species in México. This diversity is higher compared to the 75 species reported across 14 European countries [63,64] and the 91 species reported in China [65]. Our findings highlight Mexico’s potential as a megadiverse country for Trichoderma species. This underscores the importance of continuing research, which could have significant implications for biodiversity studies and practical applications in agriculture and biological control.
The state of Guerrero stands out for its high volume of research articles that address the presence of Trichoderma. Intriguingly, this abundance of research does not correlate with the higher diversity or number of isolates reported for the state. However, we report a positive relationship (R = 0.76) between species diversity and abundance. This finding suggests that the extent of sampling efforts, which is reflected by the number of isolates collected, is a crucial factor in accurately assessing species diversity in each area. Studies in the literature, such as those by Trapero-Quintana et al. (2011) [66] and Chao et al. (2009) [67], explain the importance of increasing the sampling effort to improve the expected richness that can be reported in an area. The observed diversity of Trichoderma species may also be influenced by other variables, such as the season of sampling and its interactions with other organisms in the ecosystem [68]. This indicates the need for additional research on how seasonal variations in crop fields impact Trichoderma species populations.
Therefore, our study highlights the importance of comprehensive sampling strategies and acknowledges the influence of environmental factors on Trichoderma species diversity. This opens avenues for future research, especially focused on understanding the intricate relationships between Trichoderma species, their environment, and other coexisting organisms.
Regarding the presence of this fungus in ecosystems and agroecosystems, 20 crop types were reported with the presence of some species of Trichoderma. Species of Trichoderma were also reported in six types of ecosystems. The crop with the highest reported diversity indices was coffee (Coffea arabica). De Sousa et al. (2022) [69] mentioned that species from the genus Trichoderma are part of the microbiome present in coffee soil, and they can promote root growth and play a role in the biological control of disease. Studies such as those of Mulaw et al. (2013) [70] and Alfredo et al. (2021) [71] confirm the potential of Trichoderma in the biological control of coffee crop diseases.
In undisturbed soil, the rainforest showed the highest species richness, with 12 reported species of Trichoderma. Guzmán (1998) [72] mentions that Mexican fungal diversity is usually higher in tropical and subtropical forests than in cold, temperate, and arid zones. Studies like those of Hoyos-Carvajal et al. (2009) [41] also showed the higher species diversity of Trichoderma in tropical areas. Mexico has an extension of 315,868 km of rainforests [73]; thus, there are still unexplored areas that need to be studied. Mexico presents 34 different ecosystems, as reported by [73]. However, in this document, we only analyzed six ecosystems with 12 Trichoderma species reported. According to Sharma et al. (2019) [2], fungal species from the genus Trichoderma can adapt to various ecosystems due to their ability to effectively take advantage of different substrates. Samuels (1996) [74] confirmed this, emphasizing that Trichoderma can be found in diverse environments ranging from the tundra to the tropics.
This research confirmed that Trichoderma harzianum is the most abundant species in both agricultural and undisturbed soil in México compared to global studies, such as those by Jiang et al. (2016) [75], with 429 isolates, Kubicek et al. (2003) [3] with 37 isolates and Dou et al. (2019) [62], who reported 1454 isolates. Gupta et al. (2014) [76] mentioned that the higher abundance of T. harzianum can be attributed to its remarkable metabolic diversity. Its adaptability is evident in various substrates across Mexican soil, remarking this fungus’s growth capacity. T. harzianum also exhibits multiple biotechnological applications such as a fungicide, degrading pesticide molecules, remediating soils contaminated with heavy metals, and producing valuable compounds for the pharmaceutical and industrial sectors. Thus, T. harzianum has a significant biotechnological importance. Its potential applications across various sectors of the Mexican economy highlight its value not only in environmental science, but also in economic development [76,77,78].
The Chiapas state showed the highest Shannon (2.75), Margalef (4.168), and Menhinick (3.207) indices regarding the species diversity among all states. However, it is crucial to consider the context of these findings. In the systematic review, only four species were identified in Chiapas (six isolations) based on a single research article. In contrast, the data obtained from the GBIF platform showed ten species (ten isolates). This discrepancy highlights an important point: if our analysis were limited to research articles alone, Chiapas might have appeared as one of the most diverse states. González-Oreja and Lou (2012) [79] pointed out that we must be cautious when interpreting diversity indices, as making conclusions based solely on these values may not be valid.
Tabasco showed the highest number of species, with 20 species reported, followed by Veracruz, with 14 species reported. Aguirre Acosta et al. (2014) [80] indicated that Veracruz has the highest fungal diversity, followed by Jalisco and Mexico state. Tabasco and Veracruz are states with tropical climates benefiting the presence of fungi due to the conditions of high humidity and temperatures. Lodge (1997) [81] mentions that organic-degrading fungi such as Trichoderma are more likely to occur in tropical climates than temperate ones.
Trichoderma was present throughout the country, which indicates its cosmopolitan distribution across ecosystems and agroecosystems. However, there remain unsampled areas in Mexican states. There are also a few studies focused on the diversity of Trichoderma species. We found six articles carried out in the state of Guerrero; the diversity and number of isolates found in this state may not be considered exceptional. However, the number of articles does not necessarily indicate a higher number of species or isolates. The sampling effort determines the true measure of species diversity based on the number of isolates obtained during the study. To better understand the diversity of species of Trichoderma in a particular area, researchers should report the sampling effort in any research paper as a crucial step during this study. This can help to determine whether there are sample-related limitations that contribute to the observed diversity of Trichoderma species in a given area.
In this review, we found the same number of species reported by the Global Biodiversity Information Facility (GBIF) and through the data obtained from the systematic review; however, the species reported in the GBIF and the review were not the same. Furthermore, there was a significant difference in the number of isolates, with 207 versus 872, respectively. This highlights the importance of sharing data collected in the field through platforms such as GBIF. A study by Devkota et al. (2023) [27] revealed that research on fungal diversity is scarce, and increasing changes in land use have threatened the diversity of fungal species. Therefore, it is necessary to share knowledge on databases such as GBIF to contribute to the understanding of species diversity in unexplored areas and prevent further biodiversity losses. Dou et al. (2019) [62] also suggested that studying the diversity of Trichoderma species can help to better understand their distribution and promote the study of their ecology and evolution.
We found 57 species of Trichoderma through data obtained from GBIF and the systematic review of 1078 isolates in Mexico. This comprehensive data set allows us to place the diversity of the Mexican Trichoderma species in a global context. For instance, Zhang et al. (2005) [82] reported 13 species from 135 isolates in China; Jaklitsch & Volgmayr (2015) [83] obtained 90 species and 650 isolates from southern Europe and Micronesia; and Ma et al. (2020) [84] reported 23 species from 312 isolates in northern Xinjiang, China. Thus, our results contribute significantly to the collective knowledge of the Trichoderma species diversity in the world. Our data provide a comprehensive reference for the diversity of Trichoderma species in Mexico, facilitating direct comparisons and analyses with global data. This synthesis of information in a single document offers valuable insights for researchers studying Trichoderma species’ biodiversity and evolutionary trends worldwide.
An essential factor in species diversity is their identification through molecular biology. The results of Jaklitsch & Volgmayr (2015) [83] with a significantly higher number of species might be due to the use of 3 molecular markers (tef1, rpb2, acl1) since usually only 1 or 2 markers (ITS and rpb2) were used for the identification of Trichoderma species in the studies cited here.
In the systematic review, 541 isolates, corresponding to 50% of the total isolates, presented molecular identification (28 species). T. harzianum was the most abundant of the identified species, with 214 isolates. It should be noted that the data from GBIF do not mention the type of identification used.
We report that Trichoderma species occurred in both disturbed and undisturbed areas. In agricultural soil, 643 isolates with 33 species were obtained. T. harzianum is the species with the highest abundance, with 148 isolates. This is similar to the data reported by Jiang et al., 2016 [75], where T. harzianum was predominant in agricultural soil.
Concerning the number of Trichoderma species present per crop, Manzar et al. (2021) [85] obtained 19 isolates of T. asperellum and 1 of T. harzianum in Sorghum bicolor L. crops. In our study, T. longibrachiatum was reported as the most abundant species for the S. bicolor crop, with positive results for its use in the biological control of diseases [37].
Bechem & Afanga (2018) [86] found T. harzianum/H. lixxi to inhabit endophytically in Musa × paradisiaca. M. paradisiaca is reported to have seven endophytic species in Mexico, with T. crassum being the most abundant [21]. Therefore, understanding the effects and functions of Trichoderma species that are endophytically associated with crops is necessary, as endophytic species play important roles in the promotion of plant growth.
In the Juglans regia crop, T. harzianum was the only species reported [20]. Ahmad et al. (2012) [87] reported that T. harzianum successfully controlled the Phymatotrichopsis omnivora pest in the J. regia crop.
In the Malus domestica crop, four species of Trichoderma were reported, with T. gamsii being the most abundant [18]. Wang et al. (2021, 2022) [88,89] reported T. asperellum and T. virens in China on the same crop. T. gamsii had successful results in controlling apple tree rhizosphere diseases in both cases.
Kumar et al. 2012 [90] isolated three Trichoderma species, T. viride, T. virens, and T. harzianum, from the Mangifera indica L. crop. Interestingly, similar species were reported in México for the same crop [31]. These parallel findings underscore the need for more comprehensive research in Mexico, focusing specifically on Trichoderma species and their interactions with various mango species that are cultivated in the country.
Jiang et al. (2016) [75] obtained 15 species from 3 crops (corn, oats, and rice). T. asperellum was the most abundant in the corn crop (Zea mays), which differs from the patterns found in this study, where T. harzianum was the most abundant in the corn crop [16]. More studies focused on the diversity of Trichoderma species should be conducted in corn crops, especially because corn is one of the main crops involved in the diet of Mexicans [91].
In the sunflower (Helianthus annuus) crop, Kostyuchenko and Lyakh (2018) [92] found that T. viride was present at the flowering stage. This review reported T. asperellum, T. hamatum, and T. koningiopsis in this crop [47]. However, it is necessary to conduct research on the functions and interactions of Trichoderma species in this crop.
In the onion (Allium cepa) crop, Inglis et al. (2020) [93] reported the presence of eight species of Trichoderma. In this study, T. harzianum was reported in the same crop [13]. However, in Mexico, there are few reports of Trichoderma effects in this crop; again, more research should be conducted to fully understand the function and the relationships between Trichoderma species and onion crops.
Cocoa (Theobroma cacao) is a widely studied crop. Pavon and Rivas (2010) [94] reported a diversity of Trichoderma species in Venezuelan crops and obtained an abundance of 46% for T. harzianum. In Mexico, T. harzianum was reported to have an abundance of 54.9% in Cocoa crops [95]. Studies on Trichoderma’s ability as a biofertilizer or plant growth promoter still need to be conducted in a wide array of crops to assess the efficacy of this fungus.
For the peanut (Arachis hypogaea) crop, Ayyandurai et al. (2021) [96] obtained five species of Trichoderma in India. This makes this crop more diverse than the Mexican crops analyzed in this work, with the presence of one species, T. harziaum [10]. However, T. harzianum showed excellent results as a biological control for the pest Sclerotium rolfsii Sacc. More studies on the potential of Trichoderma remain to be conducted in this crop.
In the chili (Capsicum annuum) crop, Nawaz et al. (2018) [97] found nine species of Trichoderma compared to the five species reported in this work [14]. Therefore, since chili peppers are part of the Mexican diet, we should better understand more about Trichoderma’s interactions with the diversity of chili peppers in Mexico.
Coffee (Coffea arabica) was one of the crops with the most remarkable species diversity, with 12 species reported for Mexico. Eight species were found in Ethiopia, with T. harziamun and T. asperellum being the most abundant [69]. Several studies have been conducted in Mexico on Trichoderma’s effects on the biological control of pests, diseases, biofertilization, and plant growth promotion. However, the coffee industry offers other areas where the biological characteristics of Trichoderma species can be explored. For instance, Saldaña-Mendoza et al. (2021) [98] pointed out that the Trichoderma fungus can be used to degrade coffee pulp residues.
For garlic (Allium sativum) crops, the following two Trichoderma species were reported in this work: T. virens and T. viride [8]. Albarado-Marchena and Rivera Méndez (2015) [99] isolated two species, T. harzianum and asperellum, in the same crops in Costa Rica. These findings emphasize the importance of Trichoderma species as part of the microbiota that comprise the rhizosphere of garlic. However, information about Allium sativum and its interactions with the fungi of the Trichoderma genus is scarce in Mexico.
In this study, we found four species of Trichoderma in avocado (Persea americana) crops, with T. harzianum being the most abundant [7,50]. Hermosa et al. (2004) [100] reported four species for crops in Spain. In Mexico, however, more studies focused on the diversity of native Trichoderma species are needed. We urge researchers to conduct studies that delve into the diversity of native Trichoderma species in Mexico in a wide array of crops for a better understanding of the ecology of both the native and non-native species of Trichoderma.
Kashyap et al. (2017) [101] emphasized that the study of the roles of Trichoderma species in agriculture is vital since it can be an ally for the study of climate change. Thus, understanding the diversity of species present in agricultural soils opens the possibility of facing climate change using microorganisms such as the Trichoderma fungus.
We found reports of 16 species of Trichoderma in undisturbed soil with T. harzianum being the most predominant species. This result is compatible with studies such as those of Zhang et al. (2005) [82] and Dou et al. (2019) [62], who mention that this is the species with the most significant distribution in their studies.
The mountain cloud forest is one of the most diverse ecosystems in the world [102]. However, only Trichoderma ceraceum was reported in this ecosystem, according to our review [103]. Velez et al. (2021) [104] identified six morphotypes of Trichoderma in Mexican mountain cloud forests, but they did not identify these strains at the species level.
The xerophytic scrub and grassland ecosystems, characterized by high temperatures and soil of low organic matter, pose significant challenges for the growth of Trichoderma species. Despite these harsh conditions, studies like those conducted by Savin-Molina et al. (2021) [105] report the presence of Trichoderma species and how its abundance increases after the rainy season. The data obtained in this review showed a total of seven species in this ecosystem. Thus, species of Trichoderma adapted to arid zones can be helpful in fulfilling the needs of crops in desert ecosystems [47].
In the case of temperate forests, Blaszczyk et al. (2016) [106] obtained 12 species, with T. viride being the most predominant species. An analysis of the distribution of Trichoderma species showed that the following species inhabit temperate forests in Mexico: T. alutaceum, T. ghanense, T. harzianum, and T. viride, with T. harzianum and T. viride being the only species that are similar to the results of temperate forests already indicated [33,39,46].

5. Conclusions

In this study, Trichoderma harzianum appeared as the predominant species within the Trichoderma genus in Mexico. This study emphasizes the distribution of T. harzianum in 20 crops and four ecosystems.
A significant challenge in accurately assessing the diversity of Trichoderma species in Mexico stems from a combination of factors. For instance, there is a noticeable scarcity of dedicated research entities in Mexico focused on the study of the ecology of Trichoderma species. Additionally, the lack of diverse techniques for molecular identification employing various molecular markers complicates the accurate classification and understanding of the ecology and evolutions of the species that comprise this genus. Furthermore, the absence of a standardized methodology for sampling and data collection complicates cross-comparisons between studies, which are useful to infer ecological processes within the genus. All these factors hinder the development of a comprehensive and reliable database, which is crucial for the in-depth biodiversity studies of Trichoderma species in Mexico.
Computational tools are invaluable in advancing our understanding of the ecology and evolution of Trichoderma species nationally and globally. To achieve this, platforms such as GBIF play key roles. However, these tools exhibit certain limitations. One significant shortcoming is their inability to fully capture the specific characteristics of the study areas, which is crucial for comprehensive biodiversity assessments. Furthermore, the data currently available in these platforms often present errors or are incomplete, impacting the reliability of research results. To address these challenges, developing and implementing a specialized and standardized methodology to accurately manage, curate, and share data on microorganisms such as Trichoderma species on these platforms is imperative.
It is vital to accompany the results of diversity analysis with the results of soil analysis and microclimatic characteristics in the sampling area. This could give us a more integrative view of the ecological requirements of different species of Trichoderma. As a result, this could enhance our understanding of the ecology and evolution of species that comprise this genus and allow us to take better advantage of the benefits of the species that comprise this genus.
By addressing methodological and data challenges, future research can significantly advance our understanding of the ecological and evolutionary aspects of Trichoderma species in Mexico, contributing valuable insights to global biodiversity studies.
This study significantly broadens our understanding of the diverse species of the fungus of the genus Trichoderma, particularly in regions with economically important crops. These findings underscore the crucial role of Trichoderma as a biological control agent, offering insights into its various associated properties, which include its ability to induce defense responses during plant interactions and its potential as a biofertilizer in agricultural crops.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/d16010068/s1, Table S1: Systematic Review table; Table S2: GBIF table.

Author Contributions

Conceptualization, H.O.A.-Q., T.A.-B. and E.G.-S.; data collection and formal analysis, H.O.A.-Q. and E.G.-S.; methodology PRISMA E.G.-S.; writing—original H.O.A.-Q. and E.G.-S.; writing—review and editing, H.O.A.-Q., T.A.-B., E.G.-S. and Y.D.O.-H. All authors have read and agreed to the published version of the manuscript.

Funding

This work was funded by the Instituto Politécnico Nacional through project SIP-IPN. We are also grateful for the support of the Consejo Nacional de Humanidades Ciencias y Tecnologías (CONAHCYT) for awarding a grant to the first author CVU 451094 to undertake their postgraduate study in the Use and Conservation of Natural Resources and to the Sistema Nacional de Investigadoras e Investigadores (SNII-CONAHCYT).

Data Availability Statement

Not applicable.

Conflicts of Interest

The authors declare no conflicts of interest.

References

  1. Cai, F.; Druzhinina, I.S. In Honor of John Bissett: Authoritative Guidelines on Molecular Identification of Trichoderma. Fungal Divers. 2021, 107, 1–69. [Google Scholar] [CrossRef]
  2. Sharma, S.; Kour, D.; Rana, K.L.; Dhiman, A.; Thakur, S.; Thakur, P.; Thakur, S.; Thakur, N.; Sudheer, S.; Yadav, N.; et al. Chapter 3. Trichoderma: Biodiversity, Ecological Significances, and Industrial Applications. In Recent Advancement in White Biotechnology through Fungi. Fungal Biology; Yavdav, A., Mishra, S., Sing, S., Gupta, A., Eds.; Springer: Berlin/Heidelberg, Germany, 2019; pp. 85–120. [Google Scholar]
  3. Kubicek, C.P.; Bissett, J.; Druzhinina, I.; Kullnig-Gradinger, C.; Szakacs, G. Genetic and Metabolic Diversity of Trichoderma: A Case Study on South-East Asian Isolates. Fungal Genet. Biol. 2003, 38, 310–319. [Google Scholar] [CrossRef] [PubMed]
  4. Macías-Rodríguez, L.; Contreras-Cornejo, H.A.; Adame-Garnica, S.G.; del-Val, E.; Larsen, J. The Interactions of Trichoderma at Multiple Trophic Levels: Inter-Kingdom Communication. Microbiol. Res. 2020, 240, 126552. [Google Scholar] [CrossRef] [PubMed]
  5. Sharma, A.K.; Sharma, P. Trichoderma: Host Pathogen Interactions and Applications; Springer Nature Singapore Pte Ltd.: Singapore, 2020; Volume 1, p. 319. ISBN 9789811533204. [Google Scholar] [CrossRef]
  6. Sood, M.; Kapoor, D.; Kumar, V.; Sheteiwy, M.S.; Ramakrishnan, M.; Landi, M.; Araniti, F.; Sharma, A. Trichoderma: The “Secrets” of a Multitalented Biocontrol Agent. Plants 2020, 9, 762. [Google Scholar] [CrossRef]
  7. Andrade-Hoyos, P.; Silva-Rojas, H.V.; Romero-Arenas, O. Endophytic Trichoderma Species Isolated from Persea americana and Cinnamomum verum Roots Reduce Symptoms Caused by Phytophthora cinnamomi in Avocado. Plants 2020, 9, 1220. [Google Scholar] [CrossRef]
  8. Quiroz Sarmiento, V.F.; Ferrera Cerrato, R.; Alarcón, A.; María Encarnación, H.L. Antagonismo In Vitro de Cepas de Aspergillus y Trichoderma Hacia Hongos Filamentosos Que Afectan El Cultivo de Ajo. Rev. Mex. Micol. 2008, 26, 27–34. [Google Scholar]
  9. Osorio Nila, M.A.; Vázquez-García, L.M.; Salgado-Siclán, M.L.; González-Esquivel, C.E. Efecto de Dos Enmiendas Orgánicas y Trichoderma spp. Para Controlar Sclerotinia spp. En Lechuga. Rev. Chapingo Ser. Hortic. 2005, 11, 203–208. [Google Scholar] [CrossRef]
  10. Michel-Aceves, A.C.; Otero-Sánchez, M.A.; Ariza-Flores, R.; Barros-Ayala, A.; Alarcón-Cruz, N. Eficiencia Biológica de Cepas Nativas de Trichoderma spp., En El Control de Sclerotium rolfsii Sacc., En Cacahuate. Av. Investig. Agropecu. 2013, 17, 89–107. [Google Scholar]
  11. Tirado-Gallego, P.A.; Lopera-Álvarez, A.; Ríos-Osorio, L.A. Estrategias de Control de Moniliophthora roreri y Moniliophthora perniciosa En Theobroma cacao L.: Revisión Sistemática. Corpoica Cienc. Tecnol. Agropecu. Mosquera 2016, 17, 417–430. [Google Scholar] [CrossRef]
  12. Canseco Martínez, D.A.; Villegas Aparicio, Y.; Castañeda Hidalgo, E.; Carrillo Rodríguez, J.C.; Robles, C.; Santiago Martínez, G.M. Response of Coffea arabica L. to the application of organic fertilizers and biofertilizers. Rev. Mex. Cienc. Agrícolas 2020, 11, 1285–1298. [Google Scholar]
  13. Martínez-Salgado, S.J.; Andrade-Hoyos, P.; Romero-Arenas, O.; Villa-Ruano, N.; Landeta-Cortés, G.; Rivera-Tapia, J.A. Control in Vitro de Fusarium sp. Asociado al Cultivo de Cebolla Mediante Trichoderma harzianum. Rev. Mex. Fitopatol. Mex. J. Phytopathol. 2021, 39, 2. [Google Scholar] [CrossRef]
  14. López, G.; González González, C.; Andrés, P. Selección de Cepas Nativas de Trichoderma spp. Con Actividad Antagónica Sobre Phytophthora capsici Leonian y Promotoras de Crecimiento En El Cultivo de Chile (Capsicum annuum L.). Rev. Mex. Fitopatol. 2004, 22, 117–124. [Google Scholar]
  15. Hernández-Morales, J.; Romero-Rosales, T.; Michel-Aceves, A.C.; Vargas-Hernández, M.; Monteon-Ojeda, A.; Valenzuela-Lagarda, J.L. Antagonismo enzimático de Trichoderma spp., sobre Phytophthora parasitica y Fusarium oxysporum en jamaica (Hibiscus sabdariffa L.). Bioagro 2021, 33, 203–214. [Google Scholar] [CrossRef]
  16. Castro-del Ángel, E.; Sánchez-Arizpe, A.; Galindo Cepeda, M.E.; Ernesto-Vázquez Badillo, M. Trichoderma Species Effect on the Incidence by Fusarium Verticillioides in Four Maíz Genotypes. Trop. Subtrop. Agroecosyst. 2021, 67, 1–11. [Google Scholar]
  17. Sánchez-García, B.M.; Espinosa-Huerta, E.; Villordo-Pineda, E.; Rodríguez-Guerra, R.; Mora-Avilés, M.A. Trichoderma spp. Native Strains Molecular Identification and In Vitro Antagonistic Evaluation of Root Phithopathogenic Fungus of the Common Bean (Phaseolus vulgaris L.) Cv. Montcalm. Agrociencia 2017, 51, 63–79. [Google Scholar]
  18. Ruiz-Cisneros, M.F.; Rios-Velasco, C.; Berlanga-Reyes, D.I.; Ornelas-Paz, J.d.J.; Acosta-Muñiz, C.H.; Romo-Chacón, A.; Zamudio-Flores, P.B.; Pérez-Corral, D.A.; Salas-Marina, M.Á.; Ibarra-Rendón, E.; et al. Incidencia y Agentes Causales de Enfermedades de Raíz y Sus Antagonistas En Manzanos de Chihuahua, México. Rev. Mex. Fitopatol. Mex. J. Phytopathol. 2017, 35, 437–462. [Google Scholar] [CrossRef]
  19. Santos-Villalobos, S.d.l.; Guzmán-Ortiz, D.A.; Gómez-Lim, M.A.; Délano-Frier, J.P.; de-Folter, S.; Sánchez-García, P.; Peña-Cabriales, J.J. Potential Use of Trichoderma asperellum (Samuels, Liechfeldt et Nirenberg) T8a as a Biological Control Agent against Anthracnose in Mango (Mangifera indica L.). Biol. Control 2013, 64, 37–44. [Google Scholar] [CrossRef]
  20. Samaniego-Gaxiola, J.A.; Pedroza-Sandoval, A.; Chew-Madinaveitia, Y.; Gaytán-Mascorro, A. Desinfestación Reductiva, Suelo Desecado y Trichoderma Harzianum Para Controlar Phymatotrichopsis omnivora En Vivero de Nogal Pecanero. Rev. Mex. Fitopatol. Mex. J. Phytopathol. 2019, 37, 2. [Google Scholar] [CrossRef]
  21. David Maldonado Bonilla, L.; Claudia Sánchez-Espinosa, A.; Luis Villarruel-Ordaz, J. Mycoparasitic Antagonism of a Trichoderma harzianum Strain Isolated from Banana Plants in Oaxaca, Mexico. Biotecnia 2021, 23, 127–134. [Google Scholar] [CrossRef]
  22. Sánchez, V.; Rebolledo, O. Especies de Trichoderma En Suelos Cultivados Con Agave tequilana En La Región de Los Altos Sur, Jalisco y Valoración de Su Capacidad Antagónica Contra Thielaviopsis paradoxa. Rev. Mex. Micol. 2010, 32, 12–17. [Google Scholar]
  23. Hernández-Melchor, D.J.; Ferrera-Cerrato, R.; Alarcón, A. Trichoderma: Importancia Agrícola, Biotecnológica, y Sistemas de Fermentacion Para Producir Biomasa y Enzimas de Interés Industrial. Chil. J. Agric. Anim. Sci. Ex. Agro-Cienc. 2019, 35, 98–112. [Google Scholar] [CrossRef]
  24. Zafra, G.; Absalón, Á.E.; Cuevas, M.D.C.; Cortés-Espinosa, D.V. Isolation and Selection of a Highly Tolerant Microbial Consortium with Potential for PAH Biodegradation from Heavy Crude Oil-Contaminated Soils. Water Air Soil. Pollut. 2014, 225, 1826. [Google Scholar] [CrossRef]
  25. Halme, P.; Heilmann-Clausen, J.; Rämä, T.; Kosonen, T.; Kunttu, P. Monitoring Fungal Biodiversity—Towards an Integrated Approach. Fungal Ecol. 2012, 5, 750–758. [Google Scholar] [CrossRef]
  26. Page, M.J.; McKenzie, J.E.; Bossuyt, P.M.; Boutron, I.; Hoffmann, T.C.; Mulrow, C.D.; Shamseer, L.; Tetzlaff, J.M.; Akl, E.A.; Brennan, S.E.; et al. The PRISMA 2020 Statement: An Updated Guideline for Reporting Systematic Reviews. Syst. Rev. 2021, 10, 89. [Google Scholar] [CrossRef]
  27. Devkota, S.; Fang, W.; Arunachalam, K.; Phyo, K.M.M.; Shakya, B. Systematic Review of Fungi, Their Diversity and Role in Ecosystem Services from the Far Eastern Himalayan Landscape (FHL). Heliyon 2023, 9, e12756. [Google Scholar] [PubMed]
  28. Torres-De La Cruz, M.; Ortiz-García, C.F.; Bautista-Muñoz, C.; Ramírez-Pool, J.A.; Ávalos-Contreras, N.; Cappello-García, S.; De La Cruz-Pérez, A. Diversidad de Trichoderma En El Agroecosistema Cacao Del Estado de Tabasco, México. Rev. Mex. Biodivers. 2015, 86, 947–961. [Google Scholar] [CrossRef]
  29. Sánchez Hernández, L.; Arias Mota, R.M.; Rosique Gil, J.E.; Pacheco Figueroa, C.J. Diversidad del género Trichoderma (Hypocraceae) en un Área Natural Protegida en Tabasco, México. Acta Bot. Mex. 2018, 123, 167–182. [Google Scholar] [CrossRef]
  30. Hammer, Ø.; Harper, D.A.T.; Ryan, P.D. Past: Paleontological Statistics Software Package for Education and Data Analysis. Palaeontol. Electron. 2001, 4, 1. [Google Scholar]
  31. Michel, A.; Casimiro, A.; Domínguez, R.; Gutiérrez, L.; Moreno, O.; Elena, M.; Escamilla, M.; Carlos, J. Especies de Trichoderma En Suelos Cultivados Con Mango Afectados Por Escoba de Bruja y Su Potencial Inhibitorio Sobre Fusarium Oxysporum y F. Subglutinans. Rev. Mex. Fitopatol. 2001, 19, 154–160. [Google Scholar]
  32. Talavera-Ortiz, A.; Chaverri, P.; Díaz-Godínez, G.; Acosta-Urdapilleta, M.d.L.; Villegas, E.; Téllez-Téllez, M. Mycelial Inhibition of Trichoderma spp. (Hypocreaceae) Isolated from the Cultivation of Pleurotus Ostreatus (Pleurotaceae) with an Extract of Pycnoporus sp. (Polyporaceae). Acta Bot. Mex. 2020, 127. [Google Scholar] [CrossRef]
  33. Torres Preciado, C.O.; Rodríguez Alcántar, O.; Herrera-Fonseca, M.d.J.; Figueroa-García, D. Catálogo de La Micobiota Del Complejo Volcánico de Colima, México. Acta Bot. Mex. 2020, 127, e1686. [Google Scholar] [CrossRef]
  34. Osorio-Hernández, E.; Hernández-Castillo, F.D.; Gallegos-Morales, G.; Rodríguez-Herrera, R.; Castillo-Reyes, F. In-Vitro Behavior of Trichoderma spp. against Phytophthora capsici Leonian. Afr. J. Agric. Res. 2011, 6, 4594–4600. [Google Scholar]
  35. Vera-Núñez, J.A.; Luna-Martínez, F.; Barcos-Arias, M.S.; Ávila-Miranda, M.E.; Grageda-Cabrera, O.A.; Pena-Cabriales, J.J. Enhancing 15N-Uptake in Maize (Zea mays L.) by Native Trichoderma spp. Strains in Central Mexico. Afr. J. Biotechnol. 2019, 18, 478–488. [Google Scholar] [CrossRef]
  36. Ibarra Villarreal, A.L.; Parra Cota, F.I.; Yepez, E.A.; Gutiérrez Coronado, M.A.; Valdez Torres, L.C.; De los Santos Villalobos, S. Impacto Del Cambio En El Manejo Del Cultivo de Trigo de Convencional a Orgánico Sobre Las Comunidades Fúngicas Cultivables Del Suelo En El Valle Del Yaqui, México. Agrociencia 2021, 54, 643–659. [Google Scholar] [CrossRef]
  37. Larralde-Corona, C.P.; Santiago-Mena, M.R.; Sifuentes-Rincón, A.M.; Rodríguez-Luna, I.C.; Rodríguez-Pérez, M.A.; Shirai, K.; Narváez-Zapata, J.A. Biocontrol Potential and Polyphasic Characterization of Novel Native Trichoderma Strains against Macrophomina phaseolina Isolated from Sorghum and Common Bean. Appl. Microbiol. Biotechnol. 2008, 80, 167. [Google Scholar] [CrossRef] [PubMed]
  38. Toscano, L.; Montero, G.; Cervantes, L.; Stoytcheva, M.; Gochev, V.; Beltrán, M. Production and Partial Characterization of Extracellular Lipase from Trichoderma harzianum by Solid-State Fermentation. Biotechnol. Biotechnol. Equip. 2013, 27, 3776–3781. [Google Scholar] [CrossRef]
  39. Raymundo, T.; Soto-Agudelo, R.; Bautista-Hernández, S.; Morales-Campós, A.; Valenzuela, R. Catálogo de Los Ascomicetos Del Bosque Mesófilo de Montaña de Tlanchinol, Hidalgo (México). Bol. Soc. Micol. Madr. 2016, 40, 79–104. [Google Scholar]
  40. Paramo-Aguilera, L.A.; Ortega-Morales, B.O.; Narváez-Zapata, J.A. Culturable Fungi Associated with Urban Stone Surfaces in Mexico City. Electron. J. Biotechnol. 2012, 15, 4. [Google Scholar] [CrossRef]
  41. Hoyos-Carvajal, L.; Orduz, S.; Bissett, J. Genetic and Metabolic Biodiversity of Trichoderma from Colombia and Adjacent Neotropics Regions. Fungal Genet. Biol. 2009, 46, 615–631. [Google Scholar] [CrossRef]
  42. Moo-Koh, F.A.; Cristóbal Alejo, J.; Reyes Ramírez, A.; Tun Suárez, J.M.; Gamboa Angulo, M. Identificación Molecular de Aislados de Trichoderma spp. y Su Actividad Promotora En Solanum lycopersicum L. Investig. Cienc. Univ. Autónoma Aguascalientes 2017, 25, 5–11. [Google Scholar] [CrossRef]
  43. López-Valenzuela, B.E.; Armenta-Bojórquez, A.D.; Hernández-Verdugo, S.; Apodaca-Sánchez, M.A.; Samaniego-Gaxiola, J.A.; Leyva-Madrigal, K.Y.; Valdez-Ortiz, A. Selección In Vitro e Identificación de Trichoderma spp. y Bacillus spp. Nativos Para El Control de Phymatotrichopsis omnivora. Inf. Técnica Económica Agrar. 2015, 111, 310–325. [Google Scholar] [CrossRef]
  44. Montoya-Gonzalez, A.; Quijano-Vicente, G.; Morales-Maza, A.; Ortiz-Uribe, N.; Hernández-Martínez, R. Isolation of Trichoderma spp. from Desert Soil, Biocontrol Potential Evaluation and Liquid Culture Production of Conidia Using Agricultural Fertilizers. J. Fertil. Pestic. 2016, 7, 1. [Google Scholar] [CrossRef]
  45. Zúñiga-Silgado, D.; Rivera-Leyva, J.C.; Coleman, J.J.; Sánchez-Reyez, A.; Valencia-Díaz, S.; Serrano, M.; De-Bashan, L.E.; Folch-Mallol, J.L. Soil Type Affects Organic Acid Production and Phosphorus Solubilization Efficiency Mediated by Several Native Fungal Strains from Mexico. Microorganisms 2020, 8, 1337. [Google Scholar] [CrossRef]
  46. Raymundo, T.; Valenzuela, R.; García-Martínez, Y.; Bravo-Álvarez, M.A.; Ramírez-Martínez, J.C.; Bautista-Hernández, S.; Palacios-Pacheco, M.; Luna-Vega, I. Ascomycetes (Fungi) from the Relic Forest of Fagus grandifolia Subsp. Mexicana in Eastern Mexico. Phytotaxa 2019, 418, 1–41. [Google Scholar] [CrossRef]
  47. Mendoza, H.J.L.; Sánchez Pérez, I.M.; García Olivares, J.G.; Mayek Pérez, N.; González Prieto, J.M.; Quiroz Velásquez, J.D.C. Caracterización Molecular y Agronómica de Aislados de Trichoderma spp Nativos Del Noreste de México. Rev. Colomb. Biotecnol. 2011, 13, 176–185. [Google Scholar]
  48. Michel-Aceves, A.C.; Hernández-Morales, J.; Toledo-Aguilar, R.; Sabino López, J.E.; Romero-Rosales, T. Antagonistic Capacity of Native Trichoderma spp. against Phytophthora parasitica and Fusarium oxysporum Isolated from Roselle Crops. Rev. Fitotec. Mex. 2019, 42, 235–241. [Google Scholar]
  49. Del Olmo-Ruiz, M.; Cifuentes-Blanco, J.; Vidal-Gaona, G.; Rosique-Gil, E. Micromicetos Del Suelo de Una Plantación de Plátano (Musa paradisiaca) En Teapa, Tabasco, México. Rev. Mex. Biodivers. 2010, 81, 97–102. [Google Scholar] [CrossRef]
  50. Vega-Torres, M.G.; Ruiz-Cisneros, M.F.; Pérez-Corral, D.A.; Berlanga-Reyes, D.I.; Ornelas-Paz, J.D.J.; Rios-Velasco, C.; Cambero-Campos, O.J.; Estrada-Virgen, M.O.; Luna-Esquivel, G.; Denise-Revérchon, F.L. Actividad Antifúngica in Vitro de Microorganismos Antagonistas Contra Fusarium oxysporum de Rizosfera de Árboles de Aguacate En Xalisco, Nayarit, México. Rev. Mex. Fitopatol. Mex. J. Phytopathol. 2019, 37, 57–64. [Google Scholar] [CrossRef]
  51. Rios-Velasco, C.; Caro-Cisneros, J.; Berlanga-Reyes, D.; Ruíz-Cisneros, M.F.; Ornelas-Paz, J.; Salas-Marina, M.; Villalobos-Pérez, E.; Guerrero-Prieto, V. Identification and Antagonistic Activity in Vitro of Bacillus spp. and Trichoderma spp. Isolates against Common Phytopathogenic Fungi. Rev. Mex. Fitopatol. Mex. J. Phytopathol. 2015, 34, 1. [Google Scholar] [CrossRef]
  52. Guigón-lópez, C.; Guerrero-prieto, V.; Investigación, C.D.; Cuauhtémoc, P.C.; Cp, M.; Vargas-albores, F.; Carvajal-millán, E.; Investigación, C.D.; Hermosillo, U.; Hermosillo, A.P.; et al. Identificación Molecular de Cepas Nativas de Trichoderma spp. Su Tasa de Crecimiento In Vitro y Antagonismo Contra Hongos Fitopatogenos. Rev. Mex. Fitopatol. 2010, 28, 87–96. [Google Scholar]
  53. Guadalupe, H.; Roberto, Á.; Rosa, M.; Jorge, C.; Ernesto, C. Morphological and Molecular Characterization of Native Isolates of Trichoderma and Its Potential Biocontrol against Phytophthora infestans. Rev. Mex. Fitopatol. 2017, 58–79. [Google Scholar] [CrossRef]
  54. Sánchez López, V.; Martínez Bolaños, L.; Zavala González, E.A.; Ramirez Lepe, M. Nuevos Registros de Trichoderma crassum Para México y Su Variación Morfológica En Diferentes Ecosistemas. Rev. Mex. Micol. 2012, 36, 17–26. [Google Scholar]
  55. Moreno-Pérez, P.; Gamboa-Angulo, M.; Gabriela, H.; Canto-Canché, B.; Rosado-Vallado, M.; Medina-Baizabal, I.L.; Rapa-Tussell, R. Antagonistic Properties of Micromycetes Isolated from Sinkholes of the Yucatán Peninsula against Fungal Phytopathogens. Rev. Mex. Micol. 2014, 40, 27–36. [Google Scholar]
  56. Francisco-Francisco, N.; Ortega-Ortiz, H.; Benavides-Mendoza, A.; Ramirez, H.; Fuentes-Lara, L.O.; Robledo-Torres, V. Inmovilizacion de Trichoderma harzianum En Hidrogeles de Quitosano y Su Uso En Tomate (Solanum lycopersicum). Terra Latinoam. 2012, 30, 47–57. [Google Scholar]
  57. Romero-Rosales, T.; Acuña-Soto, J.; Azuara-Domínguez, A.; Lázaro-Dzul, M.O.; Monteon-Ojeda, A.; Vargas-Madriz, H.; Secundino-Eusebio, Y. Identification and In Vitro Antagonism Evaluation of Native Strains of Trichoderma spp. on Phytopathogenic Fungi Associated with Chalice Spot in Jamaica (Hibiscus sabdariffa L.). Trop. Subtrop. Agroecosyst. 2021, 24, 1. [Google Scholar] [CrossRef]
  58. García Núñez, H.G.; Romero-Gómez, S.d.J.; González-Esquivel, C.E.; Naca-Bernal, E.G.; Martinez-Campos, A.R. Isolation of Native Strains of Trichoderma spp. from Horticultural Soils of the Valley of Toluca, for Potential Biocontrol of Sclerotinia. Trop. Subtrop. Agroecosyst. 2012, 15, 357–365. [Google Scholar]
  59. Manson, R.H.; Hernández-Ortiz, V.; Gallina, S. Agroecosistemas Cafetaleros de Veracruz: Biodiversidad, Manejo y Conservación; Instituto Nacional de Ecología: Oaxaca, Mexico, 2008; ISBN 970-709-112-6. [Google Scholar]
  60. Figueroa-Hernández, E.; Godínez-Montoya, L.; Rocha-Quiroz, J.; García-Núñez, R.M.; Pérez-Soto, F. Investigación En Matemáticas, Economía Ciencias Sociales y Agronomía; ECORFAN-México: Mexico City, Mexico, 2015; ISBN 9786078324774. [Google Scholar]
  61. Howell, C.R. Mechanisms Employed by Trichoderma Species in the Biological Control of Plant Diseases: The History and Evolution of Current Concepts. Plant Dis. 2003, 87, 4–10. [Google Scholar] [CrossRef] [PubMed]
  62. Dou, K.; Gao, J.; Zhang, C.; Yang, H.; Jiang, X.; Li, J.; Li, Y.; Wang, W.; Xian, H.; Li, S.; et al. Trichoderma Biodiversity in Major Ecological Systems of China. J. Microbiol. 2019, 57, 668–675. [Google Scholar] [CrossRef]
  63. Jaklitsch, W.M. European Species of Hypocrea Part II: Species with Hyaline Ascospores. Fungal Divers. 2011, 48, 1–250. [Google Scholar] [CrossRef]
  64. Jaklitsch, W.M. European Species of Hypocrea Part I. The Green-Spored Species. Stud. Mycol. 2009, 63, 1–91. [Google Scholar] [CrossRef]
  65. Sun, R.; Liu, Z.; Fu, K.; Fan, L.; Chen, J. Trichoderma Biodiversity in China. J. Appl. Genet. 2012, 53, 343–354. [Google Scholar] [CrossRef] [PubMed]
  66. Trapero-Quintana, A.; Reyes-Tur, B.; Araújo, N.C. Esfuerzo de Muestreo Necesario Para Estimar La Riqueza Específica Máxima En Tres Comunidades de Odonata En Cuba Empleando Exuvias. Boletín Soc. Entomológica Aragonesa 2011, 49, 285–290. [Google Scholar]
  67. Chao, A.; Colwell, R.K.; Lin, C.-W.; Gotelli, N.J. Sufficient Sampling for Asymptotic Minimum Species Richness Estimators. Ecology 2009, 90, 1125–1133. [Google Scholar] [CrossRef] [PubMed]
  68. Widden, P.; Abitbol, J.-J. Seasonality of Trichoderma Species in a Spruce-Forest Soil. Mycologia 1980, 72, 775–784. [Google Scholar] [CrossRef]
  69. de Sousa, L.P.; Guerreiro-Filho, O.; Mondego, J.M.C. The Rhizosphere Microbiomes of Five Species of Coffee Trees. Microbiol. Spectr. 2022, 10, 2. [Google Scholar] [CrossRef] [PubMed]
  70. Mulaw, T.B.; Druzhinina, I.S.; Kubicek, C.P.; Atanasova, L. Novel Endophytic Trichoderma spp. Isolated from Healthy Coffea arabica Roots Are Capable of Controlling Coffee Tracheomycosis. Diversity 2013, 5, 750–766. [Google Scholar] [CrossRef]
  71. Alfredo, L.; Rodrigo, Y.; Mamani-Huayhua, G.; Alfredo Palao-Iturregui, L.; Rodrigo Borja-Loza, Y.; Leon-Ttacca, B. Biocontrol of Coffee Yellow Rust (Hemileia vastatrix Berk. & Br.) with Trichoderma sp. Endophyte Strains. Cultiv. Trop. 2021, 42, 1. [Google Scholar]
  72. Guzmán, G. Inventorying the Fungi of Mexico. Biodivers. Conserv. 1998, 7, 369–384. [Google Scholar] [CrossRef]
  73. CONABIO. Ecosistemas de México Biodiversidad Mexicana. Available online: https://www.biodiversidad.gob.mx/ecosistemas/ecosismex (accessed on 25 December 2023).
  74. Samuels, G.J. Trichoderma: A Review of Biology and Systematics of the Genus. Mycol. Res. 1996, 100, 923–935. [Google Scholar] [CrossRef]
  75. Jiang, Y.; Wang, J.-L.; Chen, J.; Mao, L.-J.; Feng, X.-X.; Zhang, C.-L.; Lin, F.-C. Trichoderma Biodiversity of Agricultural Fields in East China Reveals a Gradient Distribution of Species. PLoS ONE 2016, 11, e0160613. [Google Scholar] [CrossRef]
  76. Gupta, V.K.; Schmoll, M.; Herrera-Estrella, A.; Upadhyay, R.S.; Druzhinina, I.; Tuohy, M.G. Biotechnology and Biology of Trichoderma; Elsevier: Amsterdam, The Netherlands, 2014; Volume 1, ISBN 9780444595768. [Google Scholar] [CrossRef]
  77. Gómez, I.; Chet, I.; Herrera-Estrella, A. Genetic Diversity and Vegetative Compatibility among Trichoderma harzianum Isolates. Mol. Gen. Genet. 1997, 256, 127–135. [Google Scholar] [CrossRef] [PubMed]
  78. Guo, R.; Li, G.; Zhang, Z.; Peng, X. Structures and Biological Activities of Secondary Metabolites from Trichoderma harzianum. Mar. Drugs 2022, 20, 701. [Google Scholar] [CrossRef]
  79. González-Oreja, J.A.; Lou, J. Midiendo La Diversidad Biológica: Más Allá Del Índice de Shannon. Acta Zoológica Lilloana 2012, 56, 3–14. [Google Scholar]
  80. Aguirre-Acosta, E.; Ulloa, M.; Aguilar, S.; Cifuentes, J.; Valenzuela, R. Biodiversidad de Hongos En México. Rev. Mex. Biodivers. 2014, 85, 76–81. [Google Scholar] [CrossRef]
  81. Lodge, D.J. Factors Related to Diversity of Decomposer Fungi in Tropical Forests. Biodivers. Conserv. 1997, 6, 681–688. [Google Scholar] [CrossRef]
  82. Zhang, C.; Druzhinina, I.S.; Kubicek, C.P.; Xu, T. Trichoderma Biodiversity in China: Evidence for a North to South Distribution of Species in East Asia. FEMS Microbiol. Lett. 2005, 251, 251–257. [Google Scholar] [CrossRef]
  83. Jaklitsch, W.M.; Voglmayr, H. Biodiversity of Trichoderma (Hypocreaceae) in Southern Europe and Macaronesia. Stud. Mycol. 2015, 80, 1–87. [Google Scholar] [CrossRef]
  84. Ma, J.; Tsegaye, E.; Li, M.; Wu, B.; Jiang, X. Biodiversity of Trichoderma from Grassland and Forest Ecosystems in Northern Xinjiang, China. 3 Biotech 2020, 10, 362. [Google Scholar] [CrossRef]
  85. Manzar, N.; Singh, Y.; Kashyap, A.S.; Sahu, P.K.; Rajawat, M.V.S.; Bhowmik, A.; Sharma, P.K.; Saxena, A.K. Biocontrol Potential of Native Trichoderma spp. against Anthracnose of Great Millet (Sorghum bicolour L.) from Tarai and Hill Regions of India. Biol. Control 2021, 152, 104474. [Google Scholar] [CrossRef]
  86. Bechem, E.T.; Afanga, Y.A. Morphological and Molecular Identification of Fungi Associated with Corm Rot and Blight Symptoms on Plantain (Musa paradisiaca) in Macro-Propagators. Int. J. Biol. Chem. Sci. 2018, 11, 2793. [Google Scholar] [CrossRef]
  87. Ahmad, M.L.; Rafiq, M.W.; Sheikh, S.; Sahay, S.; Suliman, D.M. Antagonistic Potentiality of Trichoderma harzianum against Cladosporium spherospermum, Aspergillus niger and Fusarium oxysporum. J. Biol. Agric. Healthc. 2012, 2, 72–76. [Google Scholar]
  88. Wang, H.; Tang, W.; Mao, Y.; Ma, S.; Chen, X.; Shen, X.; Yin, C.; Mao, Z. Isolation of Trichoderma virens 6PS-2 and Its Effects on Fusarium proliferatum f. Sp. Malus Domestica MR5 Related to Apple Replant Disease (ARD) in China. Hortic. Plant J. 2022. [Google Scholar] [CrossRef]
  89. Wang, H.; Zhang, R.; Duan, Y.; Jiang, W.; Chen, X.; Shen, X.; Yin, C.; Mao, Z. The Endophytic Strain Trichoderma asperellum 6s-2: An Efficient Biocontrol Agent against Apple Replant Disease in China and a Potential Plant-Growth-Promoting Fungus. J. Fungi 2021, 7, 50. [Google Scholar] [CrossRef]
  90. Kumar, P.; Misra, A.K.; Modi, D.R.; Gupta, V.K. Biocontrol Potential of Trichoderma Species against Mango Malformation Pathogens. Arch. Phytopathol. Plant Prot. 2012, 45, 1237–1245. [Google Scholar] [CrossRef]
  91. Bellon, M.R.; Berthaud, J. Traditional Mexican Agricultural Systems and the Potential Impacts of Transgenic Varieties on Maize Diversity. Agric. Hum. Values 2006, 23, 3–14. [Google Scholar] [CrossRef]
  92. Kostyuchenko, N.I.; Lyakh, V.A. Diversity of Fungi in Rhizoplane, Rhizosphere and Edaphosphere of Sunflower at Different Stages of Its Development. Helia 2018, 41, 117–127. [Google Scholar] [CrossRef]
  93. Inglis, P.W.; Mello, S.C.M.; Martins, I.; Silva, J.B.T.; Macêdo, K.; Sifuentes, D.N.; Valadares-Inglis, M.C. Trichoderma from Brazilian Garlic and Onion Crop Soils and Description of Two New Species: Trichoderma azevedoi and Trichoderma peberdyi. PLoS ONE 2020, 15, e0228485. [Google Scholar] [CrossRef]
  94. Pavone Maniscalco, D.; Rivas Cordero, M. Diversity of Trichoderma Spp. on Theobroma cacao L. Fields in Carabobo State, Venezuela, and Its Biocontrol Capacity on Crinipellis pernicosa (Stahel) Singer. Interciencia 2010, 35, 777–783. [Google Scholar]
  95. Arrazate-Argueta, V.D.C.; Martínez-Bolaños, M.; Ayala-Escobar, V.; Avendaño-Arrazate, C.H.; Hernández-Morales, J. Diversidad Morfológica y Fisiológica de Cepas Nativas de Trichoderma spp. En Suelos Cacaoteros de México. Agro Product. 2019, 12. [Google Scholar] [CrossRef]
  96. Ayyandurai, M.; Akila, R.; Manonmani, K.; Theradimani, M.; Vellaikumar, S. Phytostimulation and Growth Promotion Activities of Trichoderma spp. on Groundnut (Arachis hypogaea L.) Crop. J. Appl. Nat. Sci. 2021, 13, 1172–1179. [Google Scholar] [CrossRef]
  97. Nawaz, K.; Shahid, A.A.; Bengyella, L.; Subhani, M.N.; Ali, M.; Anwar, W.; Iftikhar, S.; Ali, S.W. Diversity of Trichoderma Species in Chili Rhizosphere That Promote Vigor and Antagonism against Virulent Phytophthora capsici. Sci. Hortic. 2018, 239, 242–252. [Google Scholar] [CrossRef]
  98. Saldaña-Mendoza, S.A.; Ascacio-Valdés, J.A.; Palacios-Ponce, A.S.; Contreras-Esquivel, J.C.; Rodríguez-Herrera, R.; Ruiz, H.A.; Martínez-Hernandez, J.L.; Sugathan, S.; Aguilar, C.N. Use of Wastes from the Tea and Coffee Industries for the Production of Cellulases Using Fungi Isolated from the Western Ghats of India. Syst. Microbiol. Biomanufacturing 2021, 1, 33–41. [Google Scholar] [CrossRef]
  99. Alvarado-Marchena, L.; Rivera-Méndez, W. Molecular Identification of Trichoderma spp. in Garlic and Onion Fields and In Vitro Antagonism Trials on Sclerotium cepivorum. Rev. Bras. Cienc. Solo 2016, 40, e0150454. [Google Scholar] [CrossRef]
  100. Hermosa, M.R.; Keck, E.; Chamorro, I.; Rubio, B.; Sanz, L.; Vizcaíno, J.A.; Grondona, I.; Monte, E. Genetic Diversity Shown in Trichoderma Biocontrol Isolates. Mycol. Res. 2004, 108, 897–906. [Google Scholar] [CrossRef] [PubMed]
  101. Kashyap, P.L.; Rai, P.; Srivastava, A.K.; Kumar, S. Trichoderma for Climate Resilient Agriculture. World J. Microbiol. Biotechnol. 2017, 33, 1–18. [Google Scholar] [CrossRef] [PubMed]
  102. Bubb, P.; May, I.; Miles, L.; Sayer, J. Cloud Forest Agenda; UNEP-WCMC: Cambridge, UK, 2004; Available online: http://www.unep-wcmc.org/resources/publications/UNEP_WCMC_bio_series/20.htm (accessed on 25 December 2023).
  103. Del Olmo-Ruiz, M.; García-Sandoval, R.; Alcántara-Ayala, O.; Véliz, M.; Luna-Vega, I. Current Knowledge of Fungi from Neotropical Montane Cloud Forests: Distributional Patterns and Composition. Biodivers. Conserv. 2017, 26, 1919–1942. [Google Scholar] [CrossRef]
  104. Velez, P.; Tapia-Torres, Y.; García-Oliva, F.; Gasca-Pineda, J. Small-Scale Variation in a Pristine Montane Cloud Forest: Evidence on High Soil Fungal Diversity and Biogeochemical Heterogeneity. PeerJ 2021, 9, e11956. [Google Scholar] [CrossRef]
  105. Savín-Molina, J.; Hernández-Montiel, L.G.; Ceiro-Catasú, W.; Ávila-Quezada, G.D.; Palacios-Espinosa, A.; Ruiz-Espinoza, F.H.; Romero-Bastidas, M. Morphological Characterization and Biocontrol Potential of Trichoderma Species Isolated from Semi-Arid Soils. Rev. Mex. Fitopatol. Mex. J. Phytopathol. 2021, 39. [Google Scholar] [CrossRef]
  106. Błaszczyk, L.; Strakowska, J.; Chełkowski, J.; Gąbka-Buszek, A.; Kaczmarek, J. Trichoderma Species Occurring on Wood with Decay Symptoms in Mountain Forests in Central Europe: Genetic and Enzymatic Characterization. J. Appl. Genet. 2016, 57, 397–407. [Google Scholar] [CrossRef]
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Figure 1. The search strategy implemented in the review and meta-analysis using the PRISMA method. This flowchart represents the searching and screening workflow, as well as the eligibility criteria applied to include/discard the documents used for the review.
Figure 1. The search strategy implemented in the review and meta-analysis using the PRISMA method. This flowchart represents the searching and screening workflow, as well as the eligibility criteria applied to include/discard the documents used for the review.
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Figure 2. Percentage of documents found in the review by areas of knowledge.
Figure 2. Percentage of documents found in the review by areas of knowledge.
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Figure 3. The number of research articles published by year that were found in the systematic review.
Figure 3. The number of research articles published by year that were found in the systematic review.
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Figure 4. The number of isolates per species found in the systematic review (SR), GBIF, and SR + GBIF combined, respectively.
Figure 4. The number of isolates per species found in the systematic review (SR), GBIF, and SR + GBIF combined, respectively.
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Figure 5. The number of Trichoderma species per state reported in this systematic review with (SR), GBIF, and SR + GBIF combined, respectively.
Figure 5. The number of Trichoderma species per state reported in this systematic review with (SR), GBIF, and SR + GBIF combined, respectively.
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Figure 6. The number of isolates per state found in this systematic review (RS) in GBIF and SR + GBIF combined, respectively.
Figure 6. The number of isolates per state found in this systematic review (RS) in GBIF and SR + GBIF combined, respectively.
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Figure 7. Species of Trichoderma present in the different crops reported in the systematic review (x-axes represent the percentage of isolates in which each species was reported). Different colors shadings in the horizontal bars correspond to the different Trichoderma species listed at the bottom of the figure.
Figure 7. Species of Trichoderma present in the different crops reported in the systematic review (x-axes represent the percentage of isolates in which each species was reported). Different colors shadings in the horizontal bars correspond to the different Trichoderma species listed at the bottom of the figure.
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Figure 8. Trichoderma species found in this review present in undisturbed soil in México (x-axes represent the percentage of isolates in which each species was present). Different color-shadings in the horizontal bars correspond to the different Trichoderma species listed at the bottom of the figure.
Figure 8. Trichoderma species found in this review present in undisturbed soil in México (x-axes represent the percentage of isolates in which each species was present). Different color-shadings in the horizontal bars correspond to the different Trichoderma species listed at the bottom of the figure.
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Figure 9. Values of the diversity indices by state calculated using the data obtained from the literature from searching electronic journals.
Figure 9. Values of the diversity indices by state calculated using the data obtained from the literature from searching electronic journals.
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Figure 10. Values of the diversity indices by state calculated using the data extracted from the GBIF platform.
Figure 10. Values of the diversity indices by state calculated using the data extracted from the GBIF platform.
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Figure 11. Values of the diversity indices by state calculated using the data obtained from electronic journals (in the systematic review) combined with the data obtained from the GBIF platform.
Figure 11. Values of the diversity indices by state calculated using the data obtained from electronic journals (in the systematic review) combined with the data obtained from the GBIF platform.
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Figure 12. Clusters obtained from the calculation of the Bray–Curtis index between states.
Figure 12. Clusters obtained from the calculation of the Bray–Curtis index between states.
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Figure 13. Values of diversity indices for the different crops analyzed in this review.
Figure 13. Values of diversity indices for the different crops analyzed in this review.
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Figure 14. Bray–Curtis clustering for crops calculated using the data obtained in this review.
Figure 14. Bray–Curtis clustering for crops calculated using the data obtained in this review.
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Figure 15. The diversity indices calculated using the data obtained through this review for undisturbed areas.
Figure 15. The diversity indices calculated using the data obtained through this review for undisturbed areas.
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Figure 16. Bray–Curtis clustering calculated using the data obtained from this review for undisturbed areas, calculated using the PAST software package.
Figure 16. Bray–Curtis clustering calculated using the data obtained from this review for undisturbed areas, calculated using the PAST software package.
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Table 1. Journals and articles found in the systematic review.
Table 1. Journals and articles found in the systematic review.
JournalArticles
Acta Botánica Mexicana[29,32,33]
African Journal of Agricultural Research[34]
African Journal of Biotechnology[35]
Agrociencia[17,36]
Applied Microbiology and Biotechnology[37]
Avances en Investigación Agropecuaria[10]
Bioagro[15]
Biological control[19]
Biotechnology & Biotechnological Equipment[38]
Revista de Ciencias Biológicas y de la Salud[21]
Boletin de la Sociedad Micológica de Madrid[39]
Electronic Journal of Biotechnology[40]
Fungal Genetics and Biology[41]
Investigación y Ciencia de la Universidad Autónoma de Aguascalientes[42]
información Técnica Económica Agraria[43]
Journal of Fertilizers and Pesticides[44]
Microorganisms[45]
Phytotaxa[46]
Plants[7]
Revista Colombiana de Biotecnología[47]
Revista Fitotecnia Mexicana[48]
Revista Mexicana de Biodiversidad[28,49]
Revista Mexicana de Fitopatología[18,31,50,51,52,53]
Revista Mexicana de Micología[8,22,54,55]
Terra Latinoamericana[56]
Tropical and Subtropical Agroecosystems[57,58]
Water, Air Soil Pollution[24]
Book: Agroecosistemas cafetaleros de Veracruz: biodiversidad, manejo y conservación[59]
Book: Investigación en Matemáticas, Economía, Ciencias sociales y Agronomía[60]
Table 2. The number of articles, total isolates, and species of the genus Trichoderma found by state in the systematic review and the GBIF platform.
Table 2. The number of articles, total isolates, and species of the genus Trichoderma found by state in the systematic review and the GBIF platform.
StatesSystematic ReviewGBIF
Number of ArticlesNumber of IsolatesSNumber of IsolatesS
Aguascalientes---75
Baja California11111
Baja California Sur166--
Campeche---33
Mexico City13311
Chiapas1421010
Chihuahua de Zaragoza326533
Coahuila2324--
Colima29332
Durango---3113
Mexico state192147
Guanajuato3465--
Guerrero736711
Hidalgo353--
Jalisco4137102
Michoacan2845711
Morelos2105--
Nayarit143--
Oaxaca317355
Puebla22211
Quintana Roo19286
San Luis Potosi---2710
Sinaloa133--
Sonora252--
Tabasco431817178
Tamaulipas212711
Tlaxcala221--
Veracruz32881411
Yucatan25365
“-” Not applicable, “S” species of the genus Trichoderma.
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Ahedo-Quero, H.O.; Aquino-Bolaños, T.; Ortiz-Hernández, Y.D.; García-Sánchez, E. Trichoderma Diversity in Mexico: A Systematic Review and Meta-Analysis. Diversity 2024, 16, 68. https://doi.org/10.3390/d16010068

AMA Style

Ahedo-Quero HO, Aquino-Bolaños T, Ortiz-Hernández YD, García-Sánchez E. Trichoderma Diversity in Mexico: A Systematic Review and Meta-Analysis. Diversity. 2024; 16(1):68. https://doi.org/10.3390/d16010068

Chicago/Turabian Style

Ahedo-Quero, Hector Osvaldo, Teodulfo Aquino-Bolaños, Yolanda Donají Ortiz-Hernández, and Edgar García-Sánchez. 2024. "Trichoderma Diversity in Mexico: A Systematic Review and Meta-Analysis" Diversity 16, no. 1: 68. https://doi.org/10.3390/d16010068

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