Diversity of endophytic fungi in the leaflets and branches of <i>Poincianella pyramidalis</i>, an endemic species of Brazilian tropical dry forest

Oliveira, Thays G. L.; Bezerra, Jadson D. P.; Silva, Iolanda R. da; Souza-Motta, Cristina M.; Magalhães, Oliane M. C.

doi:10.1590/0102-33062020abb0253

ABSTRACT

Plants harbour diverse communities of fungal species in their internal compartments. Endophytic fungi help their hosts to establish, survive, and adapt to different environments. Here, we examined the diversity of endophytic fungi in the leaflets and branches of Poincianella pyramidalis, a plant species endemic to the Brazilian tropical dry forest (Caatinga). A total of 360 fragments of leaflets and branches were analysed and 189 endophytic fungi were isolated and distributed among 21 ascomycetous genera based on their ITS and LSU rDNA sequences. Diaporthe was the most frequently identified genus, followed by Didymella and Rhytidhysteron. The colonisation rate of plant fragments was higher in the branches (74 %) than in leaflets (14 %). The richness of the genera of endophytic fungi was also higher in the branches than in leaflets, whereas no difference was observed in endophyte diversity between the plant parts, based on Shannon-Wiener and Fisher alpha diversity indices. Our results indicate that endemic plant species from Brazilian dry forest, such as P. pyramidalis, are predominantly colonised by ascomycetous fungi, especially members of the class Dothideomycetes.

Keywords: Ascomycetous fungi; Caatinga; Diaporthe; Dothideomycetes; taxonomy

Introduction

Endophytic fungi represent a large polyphyletic group of microorganisms that can reside in practically any healthy plant tissue without causing visible infections (Arnold & Herre 2003; Arnold & Lutzoni 2007; Banerjee 2011; Brader et al. 2017; Dastogeer et al. 2017). A single plant can harbour a large variety of endophytes, especially in mature tissues present in the aerial parts of the plant (Arnold 2008; Nisa et al. 2015). This symbiosis between endophytes and their plant hosts can have profound impacts on plant communities and ecosystems, leading to favourable physiological and ecological relationships for environmental balance (Hardoim et al. 2015; Brader et al. 2017). In addition, fungal endophytes can synthesise several bioactive natural products, thereby making them an important biotechnological resource (Bezerra et al. 2012, 2015; Silva et al. 2018; Pádua et al. 2019).

Endophytic diversity can be influenced by plant morphology, chemical and physiological composition, tissue type, seasons, climate conditions, and biogeographical regions (Herrera et al. 2010; Hardoim et al. 2015; Massimo et al. 2015). Most studies have focused on the diversity of endophytic fungi from temperate and humid tropical forests (Arnold & Lutzoni 2007; Banerjee 2011), whereas few studies have estimated the fungal endophyte diversity in tropical dry regions (Bezerra et al. 2012, Bezerra et al. 2017a; b; Dastogeer et al. 2017; Pádua et al. 2019; Silva et al. 2019; Bezerra et al. 2019).

The Caatinga is the largest semiarid tropical ecoregion in South America, occupying an area of 912,529 km² in Brazil (Moro et al. 2016; Silva et al. 2017). Comprising nine ecoregions, this biogeographic domain is dominated by a seasonally dry tropical forest (SDTF) influenced by low rainfall regimes (Silva et al. 2017; Pedrosa et al. 2019). Although the Caatinga presents harsh abiotic conditions (e.g., high temperatures, soil with nutrient deficiency and high salinity), this domain has an adapted biota, endemic plant and animal species, and previously undiscovered microorganisms have been found here in recent years (JC Santos et al. 2011; Silva & Souza 2018).

Poincianella pyramidalis (Fabaceae, Caesalpinioideae) (synonym Caesalpinia pyramidalis) is a plant endemic to the Caatinga which has antimicrobial, antifungal, antioxidant, anti-inflammatory, and antinociceptive properties (Cruz et al. 2007; AC Santos et al. 2011; Silva et al. 2015; Chaves et al. 2019). This species is an economically important tree for the production of firewood, fuel, alcohol, and soap. Poincianella pyramidalis easily adapts to different soil types and its populations can grow rapidly, which confers an essential role in the restoration of Caatinga ecosystems (Cabral et al. 2013; Pagotto et al. 2015; Chaves et al. 2016).

Few studies have investigated the association of fungal endophytes with P. pyramidalis, reporting the presence of seven genera (e.g. Colletotrichum, Cladosporium, Phyllosticta, Trichoderma, and Diaporthe), but without the wide taxonomic and diversity analyses of different plant tissues (Gonçalves et al. 2013; Moura et al. 2016; Sena Filho et al. 2016; Souza et al. 2016). Despite the key role of endophytic fungi in the adaptation and evolution of plant species and the maintenance of ecosystem services, limited knowledge is available regarding the diversity of microorganisms associated with endemic plant species of the Caatinga dry forest in Brazil. Thus, we tested the following hypotheses: i) the leaflets and branches of P. pyramidalis harbour a great diversity of endophytic fungi, ii) the communities of fungal endophytes differ between plant tissues, and iii) the fungal richness of P. pyramidalis can contain taxonomic novelties. To verify these hypotheses, the aim of this study was to evaluate the diversity and community structure of endophytic fungi from the leaflets and branches of P. pyramidalis, a species endemic to the Brazilian tropical dry forest (Caatinga).

Materials and methods

Study site

Samples were collected from an area of tropical dry forest (Caatinga) at the Fazenda Tamanduá (07°02'20'' S, 37°26'43'' W), a property belonging to the Mocó Agropecuária Ltda (Cabral et al. 2013), in Paraíba state. This property has an area of about 3,073 ha, of which 900 ha is part of the Private Natural Heritage Reserve of the Caatinga. The site has an average altitude of 240 m, with an average annual rainfall of 600 mm (Silva et al. 2012; Silva et al. 2014). The climate is typical of semiarid tropical regions (Bsh) according to the classification by Köppen (1948). The dominant vegetation is composed of arboreal, xerophilous, woody, and often spiny formations.

Sampling

Healthy leaflets and branches from nine individual trees of P. pyramidalis (Tul.) L. P. Queiroz up to 3 m tall were randomly collected in May 2013 during the dry season in the Caatinga. After collection, the plant material was packed into paper and nylon bags and processed within 48 h. The collection was authorised by the Ministério do Meio Ambiente (MMA)/Instituto Chico Mendes de Conservação da Biodiversidade (ICMBio); permission number: 40331-1/authentication code 87451826 issued on 4 November 2013.

Isolation of fungal endophytes

The plant material was disinfected following the same methodology used by Bezerra et al. (2015). Briefly, the leaflets and branches were first washed in tap water and neutral liquid soap, followed by disinfection using 70 % alcohol for 60 s, 2-2.5 % sodium hypochlorite for 180 s, 70 % ethanol for 30 s, and then washed three times in sterilised distilled water. Thereafter, the leaflets and branches were cut into fragments of approximately 1 cm². After disinfection, a total of 180 leaflets and 180 branch fragments (20 fragments of each plant tissue from each tree) were prepared. The fragments were transferred into Petri dishes containing potato dextrose agar (PDA) supplemented with chloramphenicol (100 mg/L) and tetracycline (50 mg/L) to inhibit bacterial growth. The plates were incubated at 28 ± 2 °C for up to 30 days. Fungal growth was observed daily, and all colonies were isolated, purified, and preserved in a solution of water and 10 % glycerol for later identification. As a control of surface disinfestation, 1 mL of water from the last wash was transferred to Petri dishes containing PDA medium supplemented with antibiotics and incubated under the same conditions.

Identification of fungal endophytes

Endophytic fungi were identified based on morphology through the observation of macro- and micro-morphological characteristics of the somatic and reproductive structures, and by DNA sequence analysis. Representative endophytic cultures are deposited in the culture collection Micoteca URM Prof. Maria Auxiliadora Cavalcanti (WCDM 604), and prepared microscopic slides in the Herbário URM Pe. Camille Torrend, both at the Universidade Federal de Pernambuco, Recife, Brazil.

DNA extraction, PCR amplification, and sequencing

Genomic DNA was extracted from pure cultures using a Wizard® SV Genomic DNA Purification System Extraction Kit (Promega) following the manufacturer's instructions. Two loci were studied, and the primers ITS1/ITS4 (White et al. 1990) and LR0R/LR5 (Vilgalys & Hester 1990; Vilgalys & Sun 1994) were used to amplify part of the internal transcribed spacer (ITS) and nuclear ribosomal small subunit (LSU) regions of the rDNA, respectively. Amplification reactions were performed following the methodology described by Bezerra et al. (2017b). Amplicon purification and sequencing reactions were performed as described by Silva et al. (2019).

Phylogenetic analyses

The sequences obtained were initially compared with corresponding sequences deposited in GenBank using the BLASTn tool, later aligned with selected sequences using the MAFFT v. 6 online interface (Katoh & Toh 2010) and edited in MEGA v. 7 (Kumar et al. 2016). Maximum Likelihood (ML) and Bayesian Inference (BI), and the analyses were performed on the CIPRES Scientific Portal (Miller et al. 2010). For ML analyses, RAxML-HPC BlackBox (8.2.12) (Stamatakis 2008) was used within the GTR+I+G standard nucleotide substitution model. The BI analysis (1 × 10⁶ generations) was performed on MrBayes at the XSEDE (CIPRES) using the nucleotide substitution model generated by the MrBayes 3.1.2 (Ronquist & Huelsenbeck 2003). The models were estimated separately for each gene region (ITS = GTR+I+G and LSU = GTR+G). The obtained trees were visualised using FigTree v.1.4.0 (Rambaut 2012). The DNA sequences generated in this study were deposited in the GenBank database of the NCBI (ITS: MN912308-MN912350 and LSU: MN912266-MN912307, Tab. S1 in material supplementary), and the alignment was deposited in TreeBASE (study ID 25646).

Colonization rate, absolute and relative frequencies

The colonisation rate (TC %) was calculated as the ratio between the number of fungal growth fragments (Nf) and the total number of fragments (Nt) (FI = Nf / Nt × 100) (Araújo et al. 2002). The relative frequency (RF) of isolation was calculated as the ratio between the number of isolates of a species to the total number of isolates (Photita et al. 2001).

Ecological data analyses

The abundance of fungal families among the leaflet and branch samples were compared using the package ‘phyloseq’ (McMurdie & Holmes 2013) and the graph was generated with the ‘ggplot2’ package (Wickham 2016). The Shannon-Wiener diversity index was calculated by the equation H' = -Σ (Pi ln (Pi)), where Pi = ni / N, ni = number of endophytic isolates, and N = total number of endophytic isolates. At the end of the analysis, H' values were converted to Exp (H'). Richness was determined by the number of species in each sample (Shannon & Weaver 1949). Fisher's alpha index was determined by the equation S = α * ln (l + n / α) (Fisher et al. 1943).

Based on the Bray-Curtis distance, permutation multivariate analysis of variance (PERMANOVA) was performed to test whether the endophytic fungal communities differed between plant tissues, and the variation in the composition of the endophytic fungal communities was visualised using non-metric multidimensional scaling (NMDS). Analyses were performed using relative abundance data. Species accumulation curves were determined, and the total richness was compared with the estimated richness using the Chao1 index and Jackknife to evaluate the sampling effort efficiency. For these analyses, we used the 'agricolae' (Mendiburu 2017), 'vegan' (Oksanen et al. 2018), and 'iNEXT' (Hsieh et al. 2016) packages. All statistical analyses were conducted in R v.3.5.0 (R Development Core Team 2018).

Results

A total of 189 endophytic fungi were isolated from 360 leaflet and branch fragments. However, 30 isolates (five from the leaflets and 25 from the branches) did not develop after preservation. The remaining 159 endophytes (137 from branches and 22 from leaflets) were found to be distributed in 16 families in Ascomycota (Figs. 1, 2). The colonisation rate of the plant tissue by the endophytic fungi was higher in the branches (74 %) than in the leaflets (14 %).

Figure 1
Phylogram generated from Bayesian inference (BI) analysis based on a combined LSU and ITS rDNA dataset from endophytic fungi isolated from Poincianella pyramidalis in the Caatinga forest (Brazil) and sequences obtained from GenBank. Posterior probabilities from BI above 0.95 and ML bootstrap support values above 70 % are shown near nodes. The tree was rooted to Earliella scabrosa (URM 7788 and MUCL 45097).

Figure 2
Taxonomic composition of endophytic fungi isolated from leaflet and branch samples of Poincianella pyramidalis in the Caatinga forest, Brazil.

The phylogenetic analyses, based on the sequence combination of ITS and LSU rDNA, consisted of 125 sequences comprising 1779 characters (including gaps). The phylogram grouped the endophytic fungi into 21 genera belonging to 10 orders of Ascomycota (Amphisphaeriales, Botryosphaeriales, Capnodiales, Diaporthales, Eurotiales, Hypocreales, Hysteriales, Kirschsteiniotheliales, Muyocopronales, and Pleosporales) (Fig. 1). Of the 21 genera, 13 (Caatingomyces, Camarographium, Didymella, Epicoccum, Fusarium, Kirschsteiniothelia, Lasiodiplodia, Pseudopithomyces, Phoma, Preussia, Rhytidhysteron, Trichoderma, and Truncatella) were present exclusively in the branches, five (Byssochlamys, Curvularia, Pyrenophora, Muyocopron, and Purpureocillium) were present exclusively in the leaflets, and three (Alternaria, Diaporthe, and Sarocladium) were isolated from both the branch and leaflet tissues. Diaporthe sp. and D. inconspicua were the most frequently identified taxa, and other endophytic fungi were rarely found (fr < 10 %). Overall, 10 taxa (Byssochlamys sp., Curvularia pallescens, Diaporthe miriciae, D. poincianellae, Pyrenophora sp., Kirschsteiniothelia sp., Lasiodiplodia sp., Pseudopithomyces sp., Muyocopron laterale, and Preussia sp.) were recovered only once (Tab 1).

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Table 1
Absolute (f) and relative (fr) frequency of endophytic fungi isolated from Poincianella pyramidalis leaflets and branches of Caatinga area.

The genera richness, Shannon-Wiener, and Fisher alpha diversity indices were 6.67, 1.04, and 4.88, respectively (Fig. 3). The accumulation curve of endophytic fungi did not reach stability; however, the Chao1 and Jackknife richness estimated the isolation of 31 and 30 genera, respectively (Fig. 4).

Figure 3
Boxplot indicating the richness (A) and diversity based on Shannon-Wiener (B) and Fisher indices (C) of endophytic fungi isolated from the leaflets and branches of Poincianella pyramidalis in the Caatinga forest, Brazil. Asterisks (*) indicate significantly higher values of the evaluated attribute based on one-way ANOVA. The median (central dot), quartile (box), maximum and minimum (whiskers) are shown.

Figure 4
Genera accumulation curve for endophytic fungi recovered from leaflets and branches of Poincianella pyramidalis in the Caatinga forest, Brazil, showing the observed and estimated richness based on the Chao 1 and Jackknife 1.

Discussion

So far, few studies have analysed the diversity of endophytic fungi from Caesalpinioideae species, including P. pyramidalis (Gonçalves et al. 2013; Moura et al. 2016; Sena Filho et al. 2016; Souza et al. 2016). This endophytic fungal association has been reported by Hilarino et al. (2011) in expanded and unexpanded mature leaves of Bauhinia brevipes; and by Bezerra et al. (2015) in the leaves, stems, sepals, and seeds of Bauhinia forficata in Brazil. Endophytic fungi were also isolated from the bark and stems of Paubrasilia echinata (= Caesalpinia echinata) (Campos et al. 2015). Studies on endophytic fungi associated with P. pyramidalis reported isolates of Colletotrichum, Cladosporium, Phyllosticta, Nodulisporium (Gonçalves et al. 2013), and Paecilomyces (Moura et al. 2016). Trichoderma species isolated as endophytes from P. pyramidalis were used for the treatment and biocontrol of diseases caused by Fusarium in pineapple plantations (Souza et al. 2016), and an important terpenoid with potential anti-cancer effects was reported from the endophyte Diaporthe sp. of P. pyramidalis (Sena Filho et al. 2016).

The high colonisation rate of endophytic fungi in the branches of P. pyramidalis has also been reported in other hosts (Liu et al. 2010; Bezerra et al. 2015; Russo et al. 2016). For example, Liu et al. (2010), studied the branches and leaves of 23 species of evergreen plants in China and 92 % of the recovered endophytic fungi were from the branches. In India, Sunayana et al. (2014) isolated endophytic fungi from Vitex negundo and recovered 143 isolates from bark, twig, and leaf tissues, observing a colonisation rate of 22.22 %, 22.66 %, and 21.33 %, respectively. In northern Thailand, Suwannarach et al. (2012) isolated 2,774 endophytes from the leaves and stems of Cinnamomum bejolghota and reported a colonisation rate varying between 97.8 % and 99.3 % from samples collected during the dry season, and between 94.8 % and 99.7 % from plant material collected during the rainy season. The variation in colonisation rates may be influenced by the differences in plant tissues, endophyte interactions, ecosystems, and the environmental conditions (Suwannarach et al. 2012; Sunayana et al. 2014; Hardoim et al. 2015).

The variability of environmental characteristics observed in the Caatinga may influence the richness and abundance of endophytic fungi in the branches because they last longer than the leaves (see Sun et al. 2011; Sun et al. 2012a). Most of the Caatinga flora is constituted of deciduous vegetation, which is dominated by trees that lose about 70 % of their small leaves during the dry season (Silva et al. 2017). The distribution pattern of the endophytes in the leaves is imbalanced (Cannon & Simmons 2002) and the abundance may vary according to their maturity (Arnold & Herre 2003). For example, plant tissues had a significant effect (15.1 % variation) on the composition of the fungal endophyte community in the twigs and leaves of Betula platyphylla, Quercus liaotungensis, and Ulmus macrocarpa in a mixed forest in China (Sun et al. 2012a), and evergreen plants had a higher incidence of endophytes when compared to deciduous plants (Lau et al. 2013).

Most endophytes found in P. pyramidalis belong to the genera described worldwide as endophytes (Khiralla et al. 2016; Rana et al. 2017; Verekar et al. 2017; Pádua et al. 2019), mainly belonging to Ascomycota in plants from different ecosystems (Arnold & Lutzoni 2007; Gazis & Chaverri 2010; Sunayana et al. 2014; Pádua et al. 2019). Fungal taxa, known as generalist fungi that grow rapidly in non-selective culture media, such as Diaporthe, Colletotrichum, Curvularia, and Fusarium are often found in different tropical plants (Arnold & Lutzoni 2007; Siqueira et al. 2011; Chowdhary & Kaushik 2015; Verekar et al. 2017). Also, some taxa found in this work had low frequency. Similar results showed that most tropical communities had a log-normal pattern distribution and few common rare taxa (Gazis & Chaverri 2010; Hilarino et al. 2011; Bezerra et al. 2013).

One interesting observation from our study was that the endophytes URM 7916 and URM 7917 were isolated from the branches of P. pyramidalis. These endophytic fungi were described as a new genus, Caatingomyces (type species C. brasiliensis), belonging to the family Teratosphaeriaceae (Capnodiales, Dothideomycetes) (Hyde et al. 2019). Teratosphaeriaceae comprises numerous cryptic species that can be defined phylogenetically based on the sequence analyses of ITS and LSU rDNA (Crous et al. 2009; Quaedvlieg et al. 2014). Species belonging to Teratosphaeriaceae are commonly found as phytopathogens; however, Readeriella considenianae has already been reported as endophytic fungi of Eucalyptus grandis × E. camaldulensis in South Africa (Marsberg et al. 2014). Another example is endophyte URM 7802, which was identified as Muyocopron laterale (Hernández-Restrepo et al. 2019) in a genus mainly found as saprobes and plant pathogens (Tibpromma et al. 2016; Hernández-Restrepo et al. 2019), but also as an endophyte (Bills & Polishook 1992, as Mycoleptodiscus atromaculans; Andrioli et al. 2012, as Mycoleptodiscus indicus; Bezerra et al. 2012, as isolate PF108).

The genus Diaporthe is commonly cited as an endophyte and has been found in different plant hosts that inhabit tropical as well as temperate areas. For example, Diaporthe was found as an endophyte in Bauhinia brevipes (Caesalpinioideae) (Hilarino et al. 2011), Cinnamomum bejolghota (Lauraceae) (Suwannarach et al. 2012), Trichilia elegans (Meliaceae) (Rhoden et al. 2012), Delonix regia (Fabaceae) (Zhou et al. 2014), Costus spiralis(Costaceae) (Marson-Ascêncioet al. 2014), and Myracrodruon urundeuva (Anacardiaceae) in Brazil (Pádua et al. 2019). Members of Diaporthe are cosmopolitan and are mainly found as saprobes, phytopathogens, and opportunistic pathogens (Udayanga et al. 2011; Gomes et al. 2013; Dissanayake et al. 2017). Several new species have been described in Diaporthe, including D. pseudoinconspicua and D. poincianellae, that we isolated from the branches of P. pyramidalis (Crous et al. 2018a; b). Additionally, Diaporthe presents species with the capacity to produce enzymes and other secondary metabolites (Maiquel et al. 2016; Yan et al. 2018; Pádua et al. 2019).

Some genera of endophytes reported in this study are commonly found in the leaves and branches of other hosts: species of Diaporthe, Fusarium, Lasiodiplodia, and Trichoderma are found in branches of Theobroma cacao in Brazil (Rubini et al. 2005); Alternaria and Epicoccum have been reported from the branches of Prunus cerasus in the Czech Republic (Hortová & Novotný 2011); Alternaria, Diaporthe, and Fusarium spp. have been reported from branches of Vitex rotundifolia in Taiwan (Yeh & Kirschner 2019); and Diaporthe and Phoma species were registered from the branches of Litsea cubeba in China (Wu et al. 2019). Endophytes from leaflets were mainly found isolates of Diaporthe and Alternaria from Hevea brasiliensis in Brazil (Vaz et al. 2018) and Peru (Gazis & Chaverri 2010); Alternaria, Diaporthe, and Curvularia from leaflets of Prosopis juliflora in India (Srivastava & Anandrao 2015); Byssochlamys, Curvularia, and Alternaria from leaves of Euphorbia prostate, Calotropis procera, and Catharanthus roseus in Sudan (Khiralla et al. 2016); and Sarocladium from leaves of Myracrodruon urundeuva in Brazil (Pádua et al. 2019).

Overall, the genera richness (6.67) and the Shannon-Wiener diversity index (1.04) recovered from P. pyramidalis were lower than those recorded in other studies. Analysing the endophytic mycobiota of Bauhinia forficata, Bezerra et al. (2015) recorded greater species richness (11) and a Shannon-Wiener diversity index of 2.206 in the stems, and Sunayana et al. (2014) recorded a higher Shannon-Wiener diversity index (2.48) in the twigs of Vitex negundo. Evaluating the leaves and stems of Cinnamomum bejolghota, Suwannarach et al. (2012) registered a diversity index varying between 1.598-1.924 in the dry season, and between 2.088-2.305 in the rainy season. Similar results were reported by Sun et al. (2012b), who studied 10 plant hosts from desert areas in China and recorded a low diversity of endophytic fungal communities in the stems and leaves (Shannon index = 0.59 to 1.92, Fisher-α index = 0.82 to 5.68). In the arid regions of northern Australia, Dastogeer et al. (2017) observed the diversity of endophytic fungi in Nicotiana and recorded a high alpha diversity (Shannon-Wiener diversity index (H′) = 2.61 ± 0.17) and a high frequency (60.8 %) of isolation in roots compared to the stem and leaf tissues.

This study of endophytic fungi from the leaflets and branches of P. pyramidalis in the Caatinga dry forest contributes significantly to the existing knowledge regarding fungal diversity. A difference in the endophytic community was observed between plant tissues, dominated by rare taxa. Moreover, the colonisation rate and species richness were higher in the branches than in the leaflets, demonstrating that the fungal endophyte community from P. pyramidalis forms an important and a specific mycobiome. Future studies focusing on the association of endophytes with other plants from dry tropical forests will be important for maintaining the preservation of vegetation cover, and for delineating conservation policies to protect plant hosts and fungal species in their natural environment.

Acknowledgements

We thank the Instituto Fazenda Tamanduá (Tamanduá Farm) for all logistical support provided for the study. We thank the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES, Finance Code 001), the Fundação de Amparo à Ciência e Tecnologia de Pernambuco (FACEPE), and the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) for financial support. We also would like to thank Dr. Jarcilene Silva de Almeida Cortez, Isaías de Oliveira Júnior (MSc), and the anonymous reviewers of our manuscript.

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Publication Dates

Publication in this collection
22 Mar 2021
Date of issue
Oct-Dec 2020

History

Received
30 May 2020
Accepted
13 Sept 2020

This is an open-access article distributed under the terms of the Creative Commons Attribution License

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Endophytic fungi	f	fr
Alternaria sp.	2	1.05
Byssochlamys sp.	1	0.52
Caatingomyces brasiliensis T.G.L. Oliveira, Souza-Motta, O.M.C. Magalhães & J.D.P. Bezerra	2	1.05
Camarographium sp.	3	1.58
Curvularia pallescens Boedijn	1	0.52
Curvularia sp.	3	1.58
Diaporthe inconspicua R.R. Gomes, Glienke & Crous	17	8.99
Diaporthe miriciae R.G. Shivas, S.M. Thomps. & Y.P. Tan	1	0.52
Diaporthe poincianellae T.G.L. Oliveira, O.M.C. Magalhães & J.D.P. Bezerra	1	0.52
Diaporthe pseudoinconspicua T.G.L. Oliveira, J.D.P. Bezerra, A.R. Machado, Souza-Motta & O.M.C. Magalhães	7	3.70
Diaporthe sp.	85	44.97
Didymella sp.	8	4.23
Pyrenophora sp.	1	0.52
Epicoccum nigrum Link	2	1.05
Fusarium sp.	3	1.58
Kirschsteiniothelia sp.	1	0.52
Lasiodiplodia sp.	1	0.52
Pseudopithomyces sp.	1	0.52
Muyocopron laterale (Alcorn & B. Sutton) Hern.-Restr., J.D.P. Bezerra & Crous	1	0.52
Phoma sp.	2	1.05
Preussia sp.	1	0.52
Purpureocillium lilacinum (Thom) Luangsa-ard, Houbraken, Hywel-Jones & Samson	2	1.05
Rhytidhysteron sp.	5	2.64
Sarocladium terricola (J.H. Mill., Giddens & A.A. Foster) A. Giraldo, Gené & Guarro	4	2.11
Trichoderma sp.	2	1.05
Truncatella sp.	2	1.05
Total	159

Diversity of endophytic fungi in the leaflets and branches of Poincianella pyramidalis, an endemic species of Brazilian tropical dry forest