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Article

Research article

J. Microbiol. Biotechnol. 2021; 31(3): 408-418

Published online March 28, 2021 https://doi.org/10.4014/jmb.2012.12041

Copyright © The Korean Society for Microbiology and Biotechnology.

Diversity and Plant Growth Promotion of Fungal Endophytes in Five Halophytes from the Buan Salt Marsh

Irina Khalmuratova1†, Doo-Ho Choi1†, Hyeok-Jun Yoon1, Tae-Myung Yoon2*, and Jong-Guk Kim1*

1School of Life Science and Biotechnology, Kyungpook National University, Daegu 701-701, Republic of Korea
2Department of Horticultural Science, Kyungpook National University, Daegu 41566, Republic of Korea

Correspondence to:Tae-Myung Yoon,  tmyoon@knu.ac.kr

Jong-Guk Kim,
        kimjg@knu.ac.kr  

Received: December 22, 2020; Revised: December 30, 2020; Accepted: December 31, 2020

Abstract

The diversity and plant growth-promoting ability of fungal endophytes that are associated with five halophytic plant species (Phragmites australis, Suaeda australis, Limonium tetragonum, Suaeda glauca Bunge, and Suaeda maritima) growing in the Buan salt marsh on the west coast of South Korea have been explored. About 188 fungal strains were isolated from these plant samples’ roots and were then studied with the use of the internal transcribed spacer (ITS) region (ITS1-5.8S-ITS2). The endophytic fungal strains belonged to 33 genera. Alternaria (18%) and Fusarium (12.8%), of the classes Dothideomycetes and Sordariomycetes, were most rampant in the coastal salt marsh plants. There was a higher diversity in fungal endophytes that are isolated from S. glauca Bunge than in isolates from other coastal salt marsh plants. Plant growth-promoting experiments with the use of Waito-C rice seedlings show that some of the fungal strains could encourage a more efficient growth than others. Furthermore, gibberellins (GAs) GA1, GA3, and GA9 were seen in the Sa-1-4-3 isolate (Acrostalagmus luteoalbus) culture filtrate with a gas chromatography/mass spectrometry.

Keywords: Coastal salt marsh plants, fungal endophytes, Buan salt marsh, growth promotion, gibberellin

Introduction

The world’s population is estimated to rise to 9 billion by 2050 [1]. There is a need to increase food production under less than optimal conditions due to population growth and climate change. In the mid- to late twentieth century, the cultivation efforts’ purpose is to improve crop varieties, introduce hybrids, and increase agricultural productions in terms of fertilizer, crop management practices, herbicides, water delivery systems, and pesticides resulted in the “Green Revolution” [2, 3]. Worldwide, there is a similar global challenge, leading to a need of breed-improved varieties as well as agricultural production practices [4]. The expansion of agricultural production to marginal lands and the effects of global climate change also need an increased biotic and abiotic stress tolerance and efficient nutrient utilization in crop plants for the future global food requirements to be met.

Endophytic fungi are organisms that are found anywhere (intercellularly or intracellularly in plants from nearly all genera of Kingdom Plantae). These fungi live in host plants for at least a portion of their lives without generating any immediate overt disease symptoms. These associations can encourage tissue differentiation and plant growth and can help in managing abiotic and biotic stresses to which the host plants are subjected [5, 6]. In addition, endophytic fungi may prevent pathogenic organisms and provide nutrients, benefiting the plant host [7]. These well-distributed fungi form diverse plant associations and thus constitute outstanding sources of new bioactive secondary metabolites [8]. Accordingly, there are several new bioactive compounds with insecticidal, antimicrobial, cytotoxic, and anticancer activities that have been separated from endophytic fungi recently [9, 10].

Plant signaling compounds, also called phytohormones, regulate plant responses to environmental change as well as control plant growth and development [11]. Notably, recent studies have reported that certain endophytes encourage host plant growth through the synthesis of phytohormones, for example, gibberellins (GAs), cytokinins, and indole-3-acetic acid (IAA) [12-14]. Indeed, endophytic fungi promote plant growth by secreting gibberellins in the rhizosphere of their hosts, which leads to an increase in plant biomass production as well as disease resistance. Apart from this, some endophytic fungi secrete both IAA and GAs into culture media [15].

This research surveys both distribution and diversity of fungal endophytes in a certain coastal region of Korea. We have investigated fungal isolates’ capacity to encourage growth of Waito-C rice seedlings and have identified whether secondary metabolites like gibberellins were seen in fungal culture filtrates.

Materials and Methods

Plant Materials and Sampling Sites

Healthy plants and roots of Phragmites australis, Suaeda australis, Limonium tetragonum, Suaeda glauca Bunge, and Suaeda maritima were gathered from different places in the Buan salt marsh in South Korea. The samples were carefully sealed in sterile plastic bags and were then processed in the laboratory within 24 hours of collection. The scientific names, codes, and local sites of the five plant species are listed in Table 1.

Table 1 . Geographic coordinates and scientific names of plants native to the Buan salt marsh..

NoScientific nameCodeSite of collectionHabitat
1Phragmites australisPa35°35'34.69"N / 126°36'2.42"EHalophytic
2Suaeda australisSa35°35'10.99"N / 126°32'44.70"EHalophytic
3Limonium tetragonumLt35°35'10.73"N / 126°32'51.40"EHalophytic
4Suaeda glauca BungeSu35°35'10.80"N / 126°32'51.90"EHalophytic
5Suaeda maritimaSm35°35'34.92"N / 126°36'3.95"EHalophytic



Sterilization and Isolation of Endophytes from the Roots of Halophytes

Fungal endophytes were isolated from healthy roots of halophytic plants that were gathered from the salt marsh. Each plant’s root samples were washed with tap water, cut into 2–2.5-cm-long segments, and treated with Tween 80 solution for 10 min on a shaker with 160 rotations per minute (rpm). Afterward, root segments were incubated in a solution of 1% (w/v) perchloric acid for 10 min and then rinsed with double-distilled water [16, 17]. Then, they were dehydrated for 5–6 min at a temperature of 22°C on a clean bench, and two to three root segments were placed in a 90-mm Petri plate with Hagem minimal media that contain 80 ppm streptomycin. Samples were incubated at 25°C in dark conditions until there is growth of fungi from the root segments seen [18, 19]. Lastly, pure fungal strains were separated from the root segments and were kept on potato dextrose agar at 25°C [20].

DNA Extraction, PCR Amplification, and the Identification of Fungal Strains

Fungal endophyte cultures were grown in an Erlenmeyer flask that contains 50 ml potato dextrose broth for 7–10 days at a temperature of 26°C on a shaker at 120 rpm. All the 188 lyophilized endophyte samples were known. There was a fungal genomic DNA extraction using a DNeasy Plant Mini Kit (Qiagen, USA). There was identification of fungi performed by sequencing the internal transcribed spacer (ITS) region with the universal primers ITS-1 (5′-TCCGTAGGTGAACCTGCGG-3′) and ITS-4 (5′-TCCTCCGCTTATTGATATGC-3′). Reaction cycling comprised of an initial denaturation step at 95°C for 2 min, which is then followed by 35 cycles of denaturation at 95°C for 30 sec, annealing at 55°C for 1 min, and extension at 72°C for 1 min. The final extension was done at 72°C for 7 min. PCR products were electrophoresed on agarose gels with an ethidium bromide stain and purified using the QIAquick PCR purification kit (Qiagen). The products were then sequenced with the use of the ABI PRISM BigDye terminator cycle sequencing kit (PE Biosystems, USA) on an ABI 310 DNA automated sequencer (Perkin, USA). The sequences were identified with the use of the BLAST (Basic Local Alignment Search Tool) tool of the National Center for Biotechnology Information (NCBI).

Statistical Analyses

The fungal endophytes’ diversity at the genus level was indicated by the Shannon diversity index (H’), Fisher’s alpha index (α), and Simpson’s index of diversity. Richness was assessed by Menhinick’s richness index (Dmn) and Margalef ’s index (Dmg) [21, 22]. The Menhinick’s index was calculated through the following formula: Dmm = S/N; Dmg=(S−1)/ln(N), where S is the number of genera in a sample, and N is the total number of individuals in a community. Both indices ranged from 0 to ∞.

The genus diversity was evaluated using the Shannon diversity index (H’), Fisher’s alpha index (α), and Simpson’s index of diversity [23]. Fisher’s alpha index (α) was calculated as follow; S=α·ln(1+N/α), where S is the number of genera, and N is the total number of individuals. The formula for Shannon’s diversity index is H' = -Σi=1Rpi·lnpi, where pi is the proportion of individuals found in genera i in a sample. The values of the Shannon diversity index generally range from 1.5 to 3.5. Simpson’s index of diversity (1-D) was calculated as follow; D =Σi=1Rni(ni-1)/N(N-1), where N is the total number of individuals in a sample, and ni is the number of individuals found in genera i in a sample. The magnitude of this index ranges from 0 to 1; the greater the magnitude, the greater the sample diversity.

Screening of Fungal Cultures on Waito-C rice Seedlings

To test whether the fungi have growth-promoting capacities, Waito-C rice sprouts were exposed to fungal culture filtrates. The fungal strains were grown in the Czapek Dox broth medium on a shaking incubator for 7 days at 25°C and 180 rpm and were harvested using filtration. The harvested fungal culture filtrates were immediately stored at a temperature of −70°C and then lyophilized. The lyophilized culture filtrates were then mixed together with 1 ml of distilled water. Waito-C rice grains were treated with uniconazole for 24 h to lessen gibberellins’ activity in the seed coat. The treated rice seeds were washed and soaked in distilled water until radical emergence occurs, and then the young seedlings were placed in glass tubes with 0.6% water agar medium to grow in a growth chamber [24]. Concentrated, lyophilized culture filtrates (10 microliters) from each fungal isolate were applied to apical meristems after the rice seedlings reached the two-leaf stage. Both the plant and shoot lengths of rice were seen after 1 week application and compared against rice seedlings treated with wild-type Gibberella fujikuroi, which was the positive control in this study.

Analysis of Gibberellins

Gibberellins were extracted from culture filtrates after the incubation of fungal isolates for 7 days in Czapek Dox broth medium that contains 1% (w/v) glucose and peptone. Reverse-phase C18 high-performance liquid chromatography followed by gas chromatography/mass spectrometry (GC/MS) with selected ion monitoring (SIM) investigated extracted gibberellins. Three major ions of the supplemented [2H2] gibberellin internal standards as well gibberellins were simultaneously monitored. The GC/MS data were eventually collected and investigated. The retention time was known with the use of hydrocarbon standards in calculating the Kovats retention index (KRI) value, and peak area ratios between non-deuterated and deuterated gibberellins were used for the quantification of the gibberellins [25].

Results

Identification of Endophytic Fungi

There is a total of 188 endophytic fungal strains separated from the roots of five species of plants collected from the Buan salt marsh on the west coast of South Korea. Fifty-two fungal strains from P. australis, 40 strains from S. australis, 25 strains from L. tetragonum, 41 strains from S. glauca Bunge, and 30 strains from S. maritima were isolated.

The endophytic fungi nucleotide sequences from each plant sample were deposited in the NCBI GenBank database under the accession numbers KP018214–KP018265 from P. australis, KP018266–KP018305 from S. australis, KP018306–KP018330 from L. tetragonum, KP018331–KP018371 from S. glauca Bunge, and KP018372–KP018401 from S. maritima (Table 2).

Table 2 . Identification of endophytic fungal isolates from roots of plants..

Sample No.Closely related fungal sequencesSimilarity (%)Accession No.
Pa-1-2-1Pestalotiopsis sp. 1 MJ-2014 (KJ572189)100KP018214
Pa-1-3-1Alternaria sp. BOP212b (KC771455)100KP018215
Pa-1-3-3Fusarium incarnatum strain LS 03 (KJ721990)99KP018216
Pa-1-4-3Trichoderma aureoviride strain SL (KJ610807)99KP018217
Pa-1-6-1Alternaria rosae strain CM24T-EY-E (KF815569)99KP018218
Pa-1-6-2Lewia sp. OUCMBI101191 (HQ914885)100KP018219
Pa-1-8-1Alternaria alternata strain HMA1D (KJ677246)100KP018220
Pa-1-8-2Penicillium oxalicum strain SY20-5 (KJ619622)99KP018221
Pa-1-8-3Fusarium incarnatum strain FI-00602 (KJ572780)100KP018222
Pa-1-8-4Talaromyces verruculosus (JN676121)99KP018223
Pa-1-9-1Fusarium incarnatum strain FI-00602 (KJ572780)100KP018224
Pa-1-9-2Alternaria alternata strain HMA1D (KJ677246)100KP018225
Pa-1-9-3Alternaria sp. HT-M18-LS (KJ527010)100KP018226
Pa-2-2-2Lewia sp. OUCMBI101191 (HQ914885)99KP018227
Pa-2-2-3Simplicillium obclavatum (AB604000)100KP018228
Pa-2-2-4Macrophoma sp. TXc4-6 (HQ262514)100KP018229
Pa-2-3-1Alternaria sp. DX-FOF7 (KF558883)100KP018230
Pa-2-3-4Alternaria alternata strain HMA1D (KJ677246)100KP018231
Pa-2-4-1-2Penicillium sp. CCF3828 (FJ430753)99KP018232
Pa-2-4-2Trichoderma ovalisporum strain (KC847168)100KP018233
Pa-2-5-2Penicillium sp. CCF3828 (FJ430753)99KP018234
Pa-2-6-2Alternaria alternata strain HMA1D (KJ677246)100KP018235
Pa-2-6-5Cladosporium sp. HT-Z1-V (KJ527013)100KP018236
Pa-2-7-1Phoma sp. P17E3 (JN207293)99KP018237
Pa-2-7-3Alternaria alternata strain HMA1D (KJ677246)100KP018238
Pa-2-8-1-2Fusarium caeruleum (KF887087)100KP018239
Pa-2-8-2Fusarium oxysporum strain P43 (JX045812)100KP018240
Pa-2-8-3-1Fusarium incarnatum strain LS 03 (KJ721990)100KP018241
Pa-2-9-1Verticillium saksenae (KF472156)99KP018242
Pa-2-9-2Lewia sp. OUCMBI101191 (HQ914885)100KP018243
Pa-2-9-3Sclerostagonospora phragmiticola strain (KF251230)100KP018244
Pa-2-9-4Cladosporium cladosporioides strain (KJ589558)100KP018245
Pa-2-9-5Verticillium saksenae (KF472156)99KP018246
Pa-2-9-7Lewia sp. OUCMBI101191 (HQ914885)100KP018247
Pa-2-9-8Lewia sp. OUCMBI101191 (HQ914885)100KP018248
Pa-2-10-2Fusarium longipes (HG423537)99KP018249
Pa-2-10-6Lewia sp. OUCMBI101191 (HQ914885)100KP018250
Pa-3-1-1Alternaria alternata strain HMA1D (KJ677246)100KP018251
Pa-3-1-3Fusarium longipes (HG423537)99KP018252
Pa-3-2-3Fusarium longipes (HG423537)99KP018253
Pa-3-2-4Talaromyces verruculosus (JN676121)100KP018254
Pa-3-3-1Phoma sp. P17E3 (JN207293)99KP018255
Pa-3-4-1Fusarium incarnatum strain LS 03 (KJ721990)100KP018256
Pa-3-6-2Fusarium incarnatum strain LS 03 (KJ721990)100KP018257
Pa-3-7-2Fusarium commune strain dH 23113 (JX162390)100KP018258
Pa-3-7-3Penicillium spinulosum isolate FFJC 16 (KF876837)100KP018259
Pa-3-7-4-1Cladosporium cladosporioides isolate (KJ572146)100KP018260
Pa-3-7-4-2Phoma sp. P17E3 (JN207293)99KP018261
Pa-3-9-1Fusarium commune strain dH 23113 (JX162390)100KP018262
Pa-3-10-1Lecanicillium sp. O_3_BESC_246b (KC007329)100KP018263
Pa-3-10-2Fusarium longipes (HG423537)99KP018264
Pa-3-10-3Lewia sp. OUCMBI101191 (HQ914885)100KP018265
Sa-1-3-1Fusarium oxysporum strain HPA2 (KJ677253)100KP018266
Sa-1-3-2Aspergillus brasiliensis strain HPA8 (KJ677257)100KP018267
Sa-1-4-3Acrostalagmus luteoalbus isolate AcLu2 (JQ387575)100KP018268
Sa-1-5-1Phoma sp. JX1203 (KC203049)100KP018269
Sa-1-5-2-2Phoma sp. JX1203 (KC203049)100KP018270
Sa-1-6-2Macrophoma sp. TXc4-6 (HQ262514)100KP018271
Sa-1-7-2Macrophoma sp. TXc4-6 (HQ262514)100KP018272
Sa-1-9-1Fusarium incarnatum strain FI-00602 (KJ572780)100KP018273
Sa-1-9-2Macrophoma sp. TXc4-6 (HQ262514)100KP018274
Sa-2-1-2Alternaria alternata strain HMA1D (KJ677246)100KP018275
Sa-2-2-1Exophiala oligosperma (AB480204)100KP018276
Sa-2-2-1-1Paraconiothyrium cyclothyrioides strain (KC215138)100KP018277
Sa-2-2-3Exophiala oligosperma (AB777520)100KP018278
Sa-2-3-1Macrophoma sp. TXc4-6 (HQ262514)100KP018279
Sa-2-3-2Macrophoma sp. TXc4-6 (HQ262514)100KP018280
Sa-2-4-1Pleospora bjoerlingii (JX045842)100KP018281
Sa-2-6-2Penicillium canescens strain CV0198 (JX140832)100KP018282
Sa-2-7-1Plectosphaerella sp. MF-1 (AB520859)100KP018283
Sa-2-7-2Aspergillus terreus isolate D34 (KF971363)100KP018284
Sa-2-8-1Penicillium lapidosum (KJ676451)100KP018285
Sa-2-9-1Sclerostagonospora phragmiticola strain (KF251230)99KP018286
Sa-2-9-4Paraphoma sp. BJ18 (KJ702586)100KP018287
Sa-2-10-1Macrophoma sp. TXc4-6 (HQ262514)100KP018288
Sa-2-10-2Alternaria sp. BJ35 (KJ702610)100KP018289
Sa-3-1-1Hypocrea sp. SFCF20120803-50 (KF313111)100KP018290
Sa-3-1-2Aspergillus aff. fumigatus A28 (JN246065)100KP018291
Sa-3-2-2Cladosporium sp. XJ18 (KF143793)100KP018292
Sa-3-3-1Acrostalagmus luteoalbus strain PTV-1 (GU813970)100KP018293
Sa-3-4-2Macrophoma sp. TXc4-6 (HQ262514)100KP018294
Sa-3-4-3Macrophoma sp. TXc4-6 (HQ262514)100KP018295
Sa-3-6-1Penicillium citrinum strain NF7 (KJ653821)100KP018296
Sa-3-6-3Fusarium oxysporum isolate F102 (KJ512160)100KP018297
Sa-3-8-1Penicillium simplicissimum strain (KF815055)99KP018298
Sa-3-8-1-1Alternaria sp. BJ35 (KJ702610)100KP018299
Sa-3-8-2-1Colletotrichum gloeosporioides strain (KJ632430)100KP018300
Sa-3-8-3Aspergillus sp. BJ39 (KJ702608)100KP018301
Sa-3-9-1Fusarium oxysporum isolate F102 (KJ512160)100KP018302
Sa-3-9-2Fusarium oxysporum strain HPA2 (KJ677253)99KP018303
Sa-3-10-1Penicillium citrinum strain NF7 (KJ653821)100KP018304
Sa-3-10-2Trichoderma harzianum (HG940484)100KP018305
Lt-1-1-1Pestalotiopsis sp. 1 AE-2013 strain F4872 (KF746123)100KP018306
Lt-1-2-2Pleospora bjoerlingii (JX045842)100KP018307
Lt-1-3-2Penicillium lapidosum (KJ676451)100KP018308
Lt-1-4-1Fusarium longipes (KJ412506)100KP018309
Lt-1-5-1Paraconiothyrium cyclothyrioides strain (KC215138)100KP018310
Lt-1-6-1Pleospora bjoerlingii (JX045842)100KP018311
Lt-1-8-2Alternaria alternata strain SR/I/90 (KJ767532)100KP018312
Lt-1-9-1Fusarium oxysporum f. sp. conglutinans (KF381081)100KP018313
Lt-1-10-1Pestalotiopsis clavispora strain P44 (JX045813)100KP018314
Lt-1-10-2Cochliobolus kusanoi isolate SH8 (KJ572135)100KP018315
Lt-2-1-1Colletotrichum acutatum strain 11E031 (KF717039)100KP018316
Lt-2-4-1Penicillium paneum strain M-18 (JQ422610)100KP018317
Lt-2-5-1-1Phoma sp. EIODSF018 (KJ173541)100KP018318
Lt-2-5-1-2Trichoderma sp. BCC 3579 (AY550911)99KP018319
Lt-2-6-2Penicillium sp. SK14JW2P (KC545799)100KP018320
Lt-2-7-1Alternaria sp. BJ35 (KJ702610)100KP018321
Lt-2-8-2Macrophoma sp. TXc4-6 (HQ262514)100KP018322
Lt-3-2-2Trichoderma harzianum strain ML16-1 (KJ619615)100KP018323
Lt-3-3-1Lewia sp. OUCMBI101191 (HQ914885)100KP018324
Lt-3-3-2Meira sp. JCM 18504 (AB778892)99KP018325
Lt-3-6-1Penicillium sp. 12140 (JX657339)100KP018326
Lt-3-7-1Alternaria sp. BJ35 (KJ702610)100KP018327
Lt-3-9-1Alternaria sp. BJ35 (KJ702610)99KP018328
Lt-3-9-2Aspergillus brasiliensis strain HPA8 (KJ677257)100KP018329
Lt-3-9-4Aspergillus clavatus strain USMO08 (KF669482)99KP018330
Su-1-1-1Talaromyces pinophilus isolate SCLB5 (KF913534)100KP018331
Su-1-2-1Talaromyces pinophilus isolate SCLB5 (KF913534)100KP018332
Su-1-2-2Penicillium sp. OY18307 (FJ571475)100KP018333
Su-1-4-1Hypocrea sp. SFCF20120803-50 (KF313111)100KP018334
Su-1-6-2Fusarium sp. BJ9 (KJ702598)100KP018335
Su-1-6-2-1Alternaria sp. DX-FOF7 (KF558883)100KP018336
Su-1-7-2Phomopsis sp. H4243 (GU595056)99KP018337
Su-1-10-2Alternaria sp. BJ35 (KJ702610)100KP018338
Su-2-1-1Pleospora bjoerlingii (JX045842)100KP018339
Su-2-2-3Purpureocillium lilacinum strain (KC157754)100KP018340
Su-2-3-1Phoma sp. Y19 (KJ572232)100KP018341
Su-2-3-2Pleospora bjoerlingii (JX045842)100KP018342
Su-2-4-3Purpureocillium lilacinum strain (KC157756)100KP018343
Su-2-5-3Aspergillus brasiliensis (KJ445022)100KP018344
Su-2-6-2Pleospora bjoerlingii (JX045842)100KP018345
Su-2-7-1Gibberella fujikuroi (KC752592)100KP018346
Su-2-7-2Penicillium sp. OY18307 (FJ571475)100KP018347
Su-2-8-1Alternaria sp. BJ35 (KJ702610)100KP018348
Su-2-8-2Metacordyceps chlamydosporia (FN598950)99KP018349
Su-2-9-1Penicillium sp. Cs/13/2 (JN585948)100KP018350
Su-2-9-2Alternaria sp. BJ35 (KJ702610)100KP018351
Su-2-9-3Macrophoma sp. TXc4-6 (HQ262514)100KP018352
Su-2-10-1Alternaria sp. 174wat (KF811432)100KP018353
Su-2-10-2Penicillium sp. KJ-2012 strain GZU(JQ965022)100KP018354
Su-3-1-1Davidiella macrospora (KJ529009)100KP018355
Su-3-1-1-1Davidiella macrospora (KJ529009)100KP018356
Su-3-1-2Pleospora bjoerlingii (JX045842)99KP018357
Su-3-3-1Fusarium oxysporum strain P43 (JX045812)100KP018358
Su-3-4-1Pestalotiopsis clavispora strain P44 (JX045813)100KP018359
Su-3-4-3Pleospora bjoerlingii (JX045842)100KP018360
Su-3-5-1Phomopsis sp. H4243 (GU595056)99KP018361
Su-3-5-2Aspergillus terreus isolate D34 (KF971363)100KP018362
Su-3-6-1Colletotrichum gloeosporioides strain (KJ632430)100KP018363
Su-3-6-3Aspergillus allahabadii strain CBS (GQ342626)100KP018364
Su-3-6-5Pestalotiopsis clavispora strain P44 (JX045813)100KP018365
Su-3-7-2Purpureocillium lilacinum strain E303 (KJ540087)100KP018366
Su-3-7-3Cladosporium sp. BJ45 (KJ702611)100KP018367
Su-3-9-1Clonostachys rosea strain F-3-51 (KF887020)100KP018368
Su-3-9-2Gliomastix murorum (AB540558)100KP018369
Su-3-10-1Alternaria sp. BJ35 (KJ702610)100KP018370
Su-3-10-2-1Colletotrichum gloeosporioides strain (KJ632430)100KP018371
Sm-1-1-2Aspergillus sp. SL-F20 (KJ528990)99KP018372
Sm-1-3-1Macrophoma sp. TXc4-6 (HQ262514)100KP018373
Sm-1-3-2Tetracladium setigerum isolate (HQ647302)99KP018374
Sm-1-5-3Macrophoma sp. TXc4-6 (HQ262514)100KP018375
Sm-1-6-2Alternaria sp. BJ35 (KJ702610)100KP018376
Sm-1-9-2-2Macrophoma sp. TXc4-6 (HQ262514)100KP018377
Sm-1-10-1Fusarium andiyazi strain CBS 134430 (KC954400)100KP018378
Sm-1-10-2Alternaria sp. BJ35 (KJ702610)100KP018379
Sm-2-1-3Alternaria sp. BJ35 (KJ702610)100KP018380
Sm-2-6-1Macrophoma sp. TXc4-6 (HQ262514)100KP018381
Sm-2-6-2Alternaria sp. BJ35 (KJ702610)100KP018382
Sm-2-7-2Macrophoma sp. TXc4-6 (HQ262514)100KP018383
Sm-2-8-1Talaromyces trachyspermus strain (KF147920)99KP018384
Sm-2-8-2-1Exophiala oligosperma (AB777520)100KP018385
Sm-2-8-2-2Meira sp. JCM 18504 (AB778892)99KP018386
Sm-2-9-1Alternaria sp. DX-FOF7 (KF558883)100KP018387
Sm-2-9-2Alternaria sp. BJ35 (KJ702610)100KP018388
Sm-2-10-1Alternaria sp. HT-M18-LS (KJ527010)100KP018389
Sm-2-10-2Cladosporium cladosporioides strain (KJ589558)100KP018390
Sm-3-1-1Macrophoma sp. TXc4-6 (HQ262514)99KP018391
Sm-3-1-3Cladosporium oxysporum strain B2F2 (KJ589590)100KP018392
Sm-3-2-1Alternaria sp. BJ35 (KJ702610)100KP018393
Sm-3-3-3Penicillium sp. JMG302 (KJ598874)98KP018394
Sm-3-4-1Cochliobolus kusanoi isolate SH8 (KJ572135)100KP018395
Sm-3-5-1Alternaria sp. DX-FOF7 (KF558883)100KP018396
Sm-3-8-1Alternaria sp. DX-FOF7 (KF558883)100KP018397
Sm-3-8-2Macrophoma sp. TXc4-6 (HQ262514)100KP018398
Sm-3-9-2Macrophoma sp. TXc4-6 (HQ262514)100KP018399
Sm-3-10-2Alternaria sp. HT-M18-LS (KJ527010)100KP018400
Sm-3-10-3Cladosporium cladosporioides strain (KJ589558)100KP018401



There was a total of 188 strains categorized into the phyla Ascomycota (186 strains) and Basidiomycota (two strains). The class Dothideomycetes (93 strains) has the largest number of strains, followed by the following classes: Sordariomycetes (56 strains), Eurotiomycetes (36 strains), Exobasidiomycetes (two strains), and Leotiomycetes (one strain). At the genus level, Alternaria has the largest proportion of isolates (34 strains) followed by Fusarium (24 strains).

The genus of each strain was observed, and each group’s proportion at the class and genus levels was assessed (Fig. 1). Dothideomycetes has the highest percentage of isolates at the class level. With the exception of isolates from S. glauca Bunge, Dothideomycetes is the majority of fungi in every plant sample. At the genus level, Alternaria was the most prevalent (18%) fungal isolate, which is followed by Fusarium (12.7%).

Figure 1. Distribution of fungal isolates in different plant samples at the class (A) and genus (B) levels. Pa, Phragmites australis; Sa, Suaeda australis; Lt, Limonium tetragonum; Su, Suaeda glauca Bunge; and Sm, Suaeda maritima.

Diversity of Endophytic Fungi isolates

About 188 culturable fungal strains were isolated from the roots of five halophytes based on colony morphologies. All endophytic fungi from halophytes belonged to 33 genera in accordance with molecular identification. Fungal isolates were then classified into 14 genera, 16 species, and 19 unclassified strains from P. australis; 17 genera, 17 species, and 17 unclassified strains from S. australis; 14 genera, 13 species, and 11 unclassified strains from L. tetragonum; 19 genera, 14 species, and 17 unclassified strains from S. glauca Bunge; and 11 genera, 7 species, and 22 unclassified strains from S. maritima (Table 3).

Table 3 . Endophytic fungi (188 strains) isolated from five plants with scientific names, plant codes, taxa of fungal strain, and number of fungal isolates..

Scientific name of plant sampleAbbreviated plant nameTaxon of fungal strainsNo. of isolates
Phragmites australisPa14 genera, 16 species52
Suaeda australisSa17 genera, 17 species40
Limonium tetragonumLt14 genera, 13 species25
Suaeda glauca BungeSu19 genera, 14 species41
Suaeda maritimaSm11 genera, 7 species30

Pa, Phragmites australis; Sa, Suaeda australis; Lt, Limonium tetragonum; Su, Suaeda glauca Bunge; and Sm, Suaeda maritima..



As regards generic diversity, S. glauca Bunge had the highest score in Shannon’s index (2.76), Fisher’s (α) (13.75), and Simpson’s index of diversity (0.970). S. maritima had the lowest scores in Shannon’s index and Fisher’s (α) (1.86 and 6.26, respectively), and P. australis had the lowest Simpson’s index of diversity (0.904). As regards generic richness, S. glauca Bunge displayed the highest scores in Menhinick’s index (2.97) and Margalef ’s index (4.85). The lowest scores in Menhinick’s and Margalef ’s indices were in P. australis (1.94) and S. maritima (2.94), respectively (Table 4).

Table 4 . Diversity indices and distribution of endophytic fungi isolated from plants native to the Buan salt marsh..

Fungal taxonPaSaLtSuSm
Acrostalagmus2
Alternaria1034611
Aspergillus4231
Cladosporium3113
Clonostachys1
Cochliobolus11
Colletotrichum112
Davidiella2
Exophiala21
Fusarium145221
Gibberella1
Gliomastix1
Hypocrea11
Lecanicillium1
Lewia71
Macrophoma18118
Meira11
Metacordyceps1
Paraconiothyrium11
Paraphoma1
Penicillium45441
Pestalotiopsis122
Phoma3211
Phomopsis2
Plectosphaerella1
Pleospora125
Purpureocillium3
Sclerostagonospora11
Simplicillium1
Talaromyces221
Tetracladium1
Trichoderma212
Verticillium2
N5240254130
S1417141911
Shannon diversity index (H')2.222.552.502.761.86
Simpson’s index of diversity (1-D)0.9040.9360.9670.9700.929
Menhinick's index (Dmn)1.942.692.802.972.01
Margalef's index (Dmg)3.294.344.044.852.94
Fisher's diversity (α)6.2911.1713.1413.756.26

Pa, Phragmites australis; Sa, Suaeda australis; Lt, Limonium tetragonum; Su, Suaeda glauca Bunge; and Sm, Suaeda maritima..



Screening for Fungal Metabolites Promoting Plant Growth in Waito-C rice Seedlings

The fungal culture filtrates were applied on Waito-C rice seedlings, and the seedling lengths were measured after 1 week of fungal culture filtrate application. Out of 188 isolated fungi, 4 fungal isolates considerably encouraged shoot lengths of rice seedlings. The fungal isolate Sa-1-4-3 promoted maximum plant and shoot lengths of 21.6 cm and 11.5 cm, respectively, while culture filtrates Pa-3-9-1, Lt-1-10-1, and Sm-3-10-2 produced plant and shoot lengths of 19.7 and 8.6 cm, 19 and 9 cm, and 21.4 and 8.6 cm, respectively. There was a much lower plant and shoot growth promotion by Gibberella fujikuroi than by Sa-1-4-3 (Fig. 2); consequently, Sa-1-4-3 was chosen for further analysis.

Figure 2. Screening for plant growth promoting of Waito-C rice seedlings with culture filtrates of fungal endophytes isolated from plant samples A-F. Ten microliters of lyophilized culture filtrates was treated to Waito-C rice seedlings. The shoot length and plant length of the Waito-C rice seedlings were measured after 7 days of treatment. The standard deviation from means was calculated using Microsoft Excel.

Extraction and Quantification of Gibberellins

After the growth of Sa-1-4-3 fungal strain for 7 days in Czapek Dox broth medium (at 25°C; 180 rpm), the culture was then filtered with the use of a filter paper to obtain a clear supernatant (150 ml). The supernatant was extracted and chromatographed for the detection of gibberellins. The GC/MS-SIM analysis has discovered that different physiologically active and inactive gibberellins have different quantities. The physiologically bioactive gibberellins were GA1 (0.285 ng/ml) and GA3 (1.479 ng/ml), while the physiologically inactive gibberellins were GA9 (0.029 ng/ml) and GA24. GA3 was considered to be more abundant than other gibberellins (Fig. 3).

Figure 3. Gibberellins content of fungal culture filtrates of the Sa-1-4-3 strain and wild type Gibberella fujikuroi. GC/MS-SIM analysis of culture filtrate extracts from the Sa-1-4-3 fungal isolate detected two bioactive GAs. Sa-1- 4-3 showed the presence of bioactivity of GA1, GA3, and other inactive GA.

Discussion

Endophytes reside inside healthy plant tissues, providing shelter and nutrition. In return, these endophytes act as an excellent source of bioactive compounds and functional metabolites that impact both plant health and growth [26-28]. Some of these metabolites prompt resistance mechanisms that protect the plants against different biotic and abiotic stresses; therefore, plant fitness and productivity are increased [29].

In our study, 188 endophytic fungi were isolated from 5 plants growing in the Buan salt marsh and were identified by ITS1, 5.8S, and ITS2 sequencing. Thirty-three genera were recognized among the isolated fungal samples. Alternaria and Fusarium were the most commonly found fungi. The majority of endophytic fungi belong to the phylum Ascomycota [30, 31]. Recent studies have reported that the genus Alternaria was the most prominent fungus found in root, stem, and leaf tissues of Gossypium hirsutum [32]. Additionally, both Alternaria and Fusarium are the most frequently encountered endophytes in different types of plants [32].

Fungal endophytes are well known for their production of a wide range of secondary metabolites and enhancement of plant resistance to environmental stress. The plant growth-enhancing effects of these fungal culture filtrates were confirmed with the use of Waito-C rice seedling bioassays [33, 34]. Although other plants are also valuable for analyze the plant growth-enhancing effects, Waito-C rice has more benefits. Because of small size of plant and lack of gibberellin, uniconazole treated Waito-C rice reacts sensitively to gibberellin from foreign substances and shows rapidly the difference in growth following injection. The use of rice mutant Waito-C, which reduces gibberellin biosynthesis, was very efficient. The Sa-1-4-3 fungal strain has promoted a better plant growth in the Waito-C rice seedlings. These results are the same as those of a previous study wherein Talaromyces pinophilus Su-3-4-3, which is isolated from the roots of S. glauca Bunge, encouraged the growth in various rice plants [35].

The host plant benefits from the hormones produced by endophytic fungi. Several studies have shown plant growth-promoting characteristics and secretion of secondary metabolites, such as gibberellins, of endophytic fungi, most of which have a relationship with the roots [34, 36]. In growth of plant, many other growth promoting compounds including cytokinins and indole-3-acetic acid are also existing. But since gibberellin is the most representative compound, it was selected as a target material for growth promotion in this study. We have acquired a strain that was initially identified as Acrostalagmus luteoalbus (Sa-1-4-3) and detected gibberellin in this culture’s filtrate. According to the result of the Waito-C rice cultivation, the A. luteoalbus strain (Sa-1-4-3) showed the better growth contribution of plant length than the G. fujikuroi. Based on the period of plant cultivation in this study, it is expected that A. luteoalbus will promote early growth of Waito-C rice in particular. The GC/MS-SIM method, an established technique to identify secondary metabolites, analyzed the gibberellins in the culture filtrate of Sa-1-4-3.

In a nutshell, a total of 188 fungi were isolated from roots of five plants that are located in the Buan salt marsh. These fungi were classified into 2 phyla, 5 classes, 10 orders, 19 families, and 33 genera. Alternaria and Fusarium accounted for more than 30% of all isolates. Endophytic fungi that are isolated from S. glauca Bunge are the most diverse. This study informs us on the capacity of A. luteoalbus (Sa-1-4-3) to produce gibberellins. These results are expected to promote plant growth in areas with high salt concentrations, which are considered to be of great benefit to crop production and agriculture.

Acknowledgments

This study was supported by the Basic Science Research Program through the National Research Foundation of Korea (NRF), Ministry of Education (2016R1A6A1A05011910), Research Institute for Dok-do and Ulleung-do Island of Kyungpook National University, and Korea Ministry of Environment as “The Eco-Innovation Project”.

Conflict of Interest


The authors have no financial conflicts of interest to declare.

Fig 1.

Figure 1.Distribution of fungal isolates in different plant samples at the class (A) and genus (B) levels. Pa, Phragmites australis; Sa, Suaeda australis; Lt, Limonium tetragonum; Su, Suaeda glauca Bunge; and Sm, Suaeda maritima.
Journal of Microbiology and Biotechnology 2021; 31: 408-418https://doi.org/10.4014/jmb.2012.12041

Fig 2.

Figure 2.Screening for plant growth promoting of Waito-C rice seedlings with culture filtrates of fungal endophytes isolated from plant samples A-F. Ten microliters of lyophilized culture filtrates was treated to Waito-C rice seedlings. The shoot length and plant length of the Waito-C rice seedlings were measured after 7 days of treatment. The standard deviation from means was calculated using Microsoft Excel.
Journal of Microbiology and Biotechnology 2021; 31: 408-418https://doi.org/10.4014/jmb.2012.12041

Fig 3.

Figure 3.Gibberellins content of fungal culture filtrates of the Sa-1-4-3 strain and wild type Gibberella fujikuroi. GC/MS-SIM analysis of culture filtrate extracts from the Sa-1-4-3 fungal isolate detected two bioactive GAs. Sa-1- 4-3 showed the presence of bioactivity of GA1, GA3, and other inactive GA.
Journal of Microbiology and Biotechnology 2021; 31: 408-418https://doi.org/10.4014/jmb.2012.12041

Table 1 . Geographic coordinates and scientific names of plants native to the Buan salt marsh..

NoScientific nameCodeSite of collectionHabitat
1Phragmites australisPa35°35'34.69"N / 126°36'2.42"EHalophytic
2Suaeda australisSa35°35'10.99"N / 126°32'44.70"EHalophytic
3Limonium tetragonumLt35°35'10.73"N / 126°32'51.40"EHalophytic
4Suaeda glauca BungeSu35°35'10.80"N / 126°32'51.90"EHalophytic
5Suaeda maritimaSm35°35'34.92"N / 126°36'3.95"EHalophytic


Table 2 . Identification of endophytic fungal isolates from roots of plants..

Sample No.Closely related fungal sequencesSimilarity (%)Accession No.
Pa-1-2-1Pestalotiopsis sp. 1 MJ-2014 (KJ572189)100KP018214
Pa-1-3-1Alternaria sp. BOP212b (KC771455)100KP018215
Pa-1-3-3Fusarium incarnatum strain LS 03 (KJ721990)99KP018216
Pa-1-4-3Trichoderma aureoviride strain SL (KJ610807)99KP018217
Pa-1-6-1Alternaria rosae strain CM24T-EY-E (KF815569)99KP018218
Pa-1-6-2Lewia sp. OUCMBI101191 (HQ914885)100KP018219
Pa-1-8-1Alternaria alternata strain HMA1D (KJ677246)100KP018220
Pa-1-8-2Penicillium oxalicum strain SY20-5 (KJ619622)99KP018221
Pa-1-8-3Fusarium incarnatum strain FI-00602 (KJ572780)100KP018222
Pa-1-8-4Talaromyces verruculosus (JN676121)99KP018223
Pa-1-9-1Fusarium incarnatum strain FI-00602 (KJ572780)100KP018224
Pa-1-9-2Alternaria alternata strain HMA1D (KJ677246)100KP018225
Pa-1-9-3Alternaria sp. HT-M18-LS (KJ527010)100KP018226
Pa-2-2-2Lewia sp. OUCMBI101191 (HQ914885)99KP018227
Pa-2-2-3Simplicillium obclavatum (AB604000)100KP018228
Pa-2-2-4Macrophoma sp. TXc4-6 (HQ262514)100KP018229
Pa-2-3-1Alternaria sp. DX-FOF7 (KF558883)100KP018230
Pa-2-3-4Alternaria alternata strain HMA1D (KJ677246)100KP018231
Pa-2-4-1-2Penicillium sp. CCF3828 (FJ430753)99KP018232
Pa-2-4-2Trichoderma ovalisporum strain (KC847168)100KP018233
Pa-2-5-2Penicillium sp. CCF3828 (FJ430753)99KP018234
Pa-2-6-2Alternaria alternata strain HMA1D (KJ677246)100KP018235
Pa-2-6-5Cladosporium sp. HT-Z1-V (KJ527013)100KP018236
Pa-2-7-1Phoma sp. P17E3 (JN207293)99KP018237
Pa-2-7-3Alternaria alternata strain HMA1D (KJ677246)100KP018238
Pa-2-8-1-2Fusarium caeruleum (KF887087)100KP018239
Pa-2-8-2Fusarium oxysporum strain P43 (JX045812)100KP018240
Pa-2-8-3-1Fusarium incarnatum strain LS 03 (KJ721990)100KP018241
Pa-2-9-1Verticillium saksenae (KF472156)99KP018242
Pa-2-9-2Lewia sp. OUCMBI101191 (HQ914885)100KP018243
Pa-2-9-3Sclerostagonospora phragmiticola strain (KF251230)100KP018244
Pa-2-9-4Cladosporium cladosporioides strain (KJ589558)100KP018245
Pa-2-9-5Verticillium saksenae (KF472156)99KP018246
Pa-2-9-7Lewia sp. OUCMBI101191 (HQ914885)100KP018247
Pa-2-9-8Lewia sp. OUCMBI101191 (HQ914885)100KP018248
Pa-2-10-2Fusarium longipes (HG423537)99KP018249
Pa-2-10-6Lewia sp. OUCMBI101191 (HQ914885)100KP018250
Pa-3-1-1Alternaria alternata strain HMA1D (KJ677246)100KP018251
Pa-3-1-3Fusarium longipes (HG423537)99KP018252
Pa-3-2-3Fusarium longipes (HG423537)99KP018253
Pa-3-2-4Talaromyces verruculosus (JN676121)100KP018254
Pa-3-3-1Phoma sp. P17E3 (JN207293)99KP018255
Pa-3-4-1Fusarium incarnatum strain LS 03 (KJ721990)100KP018256
Pa-3-6-2Fusarium incarnatum strain LS 03 (KJ721990)100KP018257
Pa-3-7-2Fusarium commune strain dH 23113 (JX162390)100KP018258
Pa-3-7-3Penicillium spinulosum isolate FFJC 16 (KF876837)100KP018259
Pa-3-7-4-1Cladosporium cladosporioides isolate (KJ572146)100KP018260
Pa-3-7-4-2Phoma sp. P17E3 (JN207293)99KP018261
Pa-3-9-1Fusarium commune strain dH 23113 (JX162390)100KP018262
Pa-3-10-1Lecanicillium sp. O_3_BESC_246b (KC007329)100KP018263
Pa-3-10-2Fusarium longipes (HG423537)99KP018264
Pa-3-10-3Lewia sp. OUCMBI101191 (HQ914885)100KP018265
Sa-1-3-1Fusarium oxysporum strain HPA2 (KJ677253)100KP018266
Sa-1-3-2Aspergillus brasiliensis strain HPA8 (KJ677257)100KP018267
Sa-1-4-3Acrostalagmus luteoalbus isolate AcLu2 (JQ387575)100KP018268
Sa-1-5-1Phoma sp. JX1203 (KC203049)100KP018269
Sa-1-5-2-2Phoma sp. JX1203 (KC203049)100KP018270
Sa-1-6-2Macrophoma sp. TXc4-6 (HQ262514)100KP018271
Sa-1-7-2Macrophoma sp. TXc4-6 (HQ262514)100KP018272
Sa-1-9-1Fusarium incarnatum strain FI-00602 (KJ572780)100KP018273
Sa-1-9-2Macrophoma sp. TXc4-6 (HQ262514)100KP018274
Sa-2-1-2Alternaria alternata strain HMA1D (KJ677246)100KP018275
Sa-2-2-1Exophiala oligosperma (AB480204)100KP018276
Sa-2-2-1-1Paraconiothyrium cyclothyrioides strain (KC215138)100KP018277
Sa-2-2-3Exophiala oligosperma (AB777520)100KP018278
Sa-2-3-1Macrophoma sp. TXc4-6 (HQ262514)100KP018279
Sa-2-3-2Macrophoma sp. TXc4-6 (HQ262514)100KP018280
Sa-2-4-1Pleospora bjoerlingii (JX045842)100KP018281
Sa-2-6-2Penicillium canescens strain CV0198 (JX140832)100KP018282
Sa-2-7-1Plectosphaerella sp. MF-1 (AB520859)100KP018283
Sa-2-7-2Aspergillus terreus isolate D34 (KF971363)100KP018284
Sa-2-8-1Penicillium lapidosum (KJ676451)100KP018285
Sa-2-9-1Sclerostagonospora phragmiticola strain (KF251230)99KP018286
Sa-2-9-4Paraphoma sp. BJ18 (KJ702586)100KP018287
Sa-2-10-1Macrophoma sp. TXc4-6 (HQ262514)100KP018288
Sa-2-10-2Alternaria sp. BJ35 (KJ702610)100KP018289
Sa-3-1-1Hypocrea sp. SFCF20120803-50 (KF313111)100KP018290
Sa-3-1-2Aspergillus aff. fumigatus A28 (JN246065)100KP018291
Sa-3-2-2Cladosporium sp. XJ18 (KF143793)100KP018292
Sa-3-3-1Acrostalagmus luteoalbus strain PTV-1 (GU813970)100KP018293
Sa-3-4-2Macrophoma sp. TXc4-6 (HQ262514)100KP018294
Sa-3-4-3Macrophoma sp. TXc4-6 (HQ262514)100KP018295
Sa-3-6-1Penicillium citrinum strain NF7 (KJ653821)100KP018296
Sa-3-6-3Fusarium oxysporum isolate F102 (KJ512160)100KP018297
Sa-3-8-1Penicillium simplicissimum strain (KF815055)99KP018298
Sa-3-8-1-1Alternaria sp. BJ35 (KJ702610)100KP018299
Sa-3-8-2-1Colletotrichum gloeosporioides strain (KJ632430)100KP018300
Sa-3-8-3Aspergillus sp. BJ39 (KJ702608)100KP018301
Sa-3-9-1Fusarium oxysporum isolate F102 (KJ512160)100KP018302
Sa-3-9-2Fusarium oxysporum strain HPA2 (KJ677253)99KP018303
Sa-3-10-1Penicillium citrinum strain NF7 (KJ653821)100KP018304
Sa-3-10-2Trichoderma harzianum (HG940484)100KP018305
Lt-1-1-1Pestalotiopsis sp. 1 AE-2013 strain F4872 (KF746123)100KP018306
Lt-1-2-2Pleospora bjoerlingii (JX045842)100KP018307
Lt-1-3-2Penicillium lapidosum (KJ676451)100KP018308
Lt-1-4-1Fusarium longipes (KJ412506)100KP018309
Lt-1-5-1Paraconiothyrium cyclothyrioides strain (KC215138)100KP018310
Lt-1-6-1Pleospora bjoerlingii (JX045842)100KP018311
Lt-1-8-2Alternaria alternata strain SR/I/90 (KJ767532)100KP018312
Lt-1-9-1Fusarium oxysporum f. sp. conglutinans (KF381081)100KP018313
Lt-1-10-1Pestalotiopsis clavispora strain P44 (JX045813)100KP018314
Lt-1-10-2Cochliobolus kusanoi isolate SH8 (KJ572135)100KP018315
Lt-2-1-1Colletotrichum acutatum strain 11E031 (KF717039)100KP018316
Lt-2-4-1Penicillium paneum strain M-18 (JQ422610)100KP018317
Lt-2-5-1-1Phoma sp. EIODSF018 (KJ173541)100KP018318
Lt-2-5-1-2Trichoderma sp. BCC 3579 (AY550911)99KP018319
Lt-2-6-2Penicillium sp. SK14JW2P (KC545799)100KP018320
Lt-2-7-1Alternaria sp. BJ35 (KJ702610)100KP018321
Lt-2-8-2Macrophoma sp. TXc4-6 (HQ262514)100KP018322
Lt-3-2-2Trichoderma harzianum strain ML16-1 (KJ619615)100KP018323
Lt-3-3-1Lewia sp. OUCMBI101191 (HQ914885)100KP018324
Lt-3-3-2Meira sp. JCM 18504 (AB778892)99KP018325
Lt-3-6-1Penicillium sp. 12140 (JX657339)100KP018326
Lt-3-7-1Alternaria sp. BJ35 (KJ702610)100KP018327
Lt-3-9-1Alternaria sp. BJ35 (KJ702610)99KP018328
Lt-3-9-2Aspergillus brasiliensis strain HPA8 (KJ677257)100KP018329
Lt-3-9-4Aspergillus clavatus strain USMO08 (KF669482)99KP018330
Su-1-1-1Talaromyces pinophilus isolate SCLB5 (KF913534)100KP018331
Su-1-2-1Talaromyces pinophilus isolate SCLB5 (KF913534)100KP018332
Su-1-2-2Penicillium sp. OY18307 (FJ571475)100KP018333
Su-1-4-1Hypocrea sp. SFCF20120803-50 (KF313111)100KP018334
Su-1-6-2Fusarium sp. BJ9 (KJ702598)100KP018335
Su-1-6-2-1Alternaria sp. DX-FOF7 (KF558883)100KP018336
Su-1-7-2Phomopsis sp. H4243 (GU595056)99KP018337
Su-1-10-2Alternaria sp. BJ35 (KJ702610)100KP018338
Su-2-1-1Pleospora bjoerlingii (JX045842)100KP018339
Su-2-2-3Purpureocillium lilacinum strain (KC157754)100KP018340
Su-2-3-1Phoma sp. Y19 (KJ572232)100KP018341
Su-2-3-2Pleospora bjoerlingii (JX045842)100KP018342
Su-2-4-3Purpureocillium lilacinum strain (KC157756)100KP018343
Su-2-5-3Aspergillus brasiliensis (KJ445022)100KP018344
Su-2-6-2Pleospora bjoerlingii (JX045842)100KP018345
Su-2-7-1Gibberella fujikuroi (KC752592)100KP018346
Su-2-7-2Penicillium sp. OY18307 (FJ571475)100KP018347
Su-2-8-1Alternaria sp. BJ35 (KJ702610)100KP018348
Su-2-8-2Metacordyceps chlamydosporia (FN598950)99KP018349
Su-2-9-1Penicillium sp. Cs/13/2 (JN585948)100KP018350
Su-2-9-2Alternaria sp. BJ35 (KJ702610)100KP018351
Su-2-9-3Macrophoma sp. TXc4-6 (HQ262514)100KP018352
Su-2-10-1Alternaria sp. 174wat (KF811432)100KP018353
Su-2-10-2Penicillium sp. KJ-2012 strain GZU(JQ965022)100KP018354
Su-3-1-1Davidiella macrospora (KJ529009)100KP018355
Su-3-1-1-1Davidiella macrospora (KJ529009)100KP018356
Su-3-1-2Pleospora bjoerlingii (JX045842)99KP018357
Su-3-3-1Fusarium oxysporum strain P43 (JX045812)100KP018358
Su-3-4-1Pestalotiopsis clavispora strain P44 (JX045813)100KP018359
Su-3-4-3Pleospora bjoerlingii (JX045842)100KP018360
Su-3-5-1Phomopsis sp. H4243 (GU595056)99KP018361
Su-3-5-2Aspergillus terreus isolate D34 (KF971363)100KP018362
Su-3-6-1Colletotrichum gloeosporioides strain (KJ632430)100KP018363
Su-3-6-3Aspergillus allahabadii strain CBS (GQ342626)100KP018364
Su-3-6-5Pestalotiopsis clavispora strain P44 (JX045813)100KP018365
Su-3-7-2Purpureocillium lilacinum strain E303 (KJ540087)100KP018366
Su-3-7-3Cladosporium sp. BJ45 (KJ702611)100KP018367
Su-3-9-1Clonostachys rosea strain F-3-51 (KF887020)100KP018368
Su-3-9-2Gliomastix murorum (AB540558)100KP018369
Su-3-10-1Alternaria sp. BJ35 (KJ702610)100KP018370
Su-3-10-2-1Colletotrichum gloeosporioides strain (KJ632430)100KP018371
Sm-1-1-2Aspergillus sp. SL-F20 (KJ528990)99KP018372
Sm-1-3-1Macrophoma sp. TXc4-6 (HQ262514)100KP018373
Sm-1-3-2Tetracladium setigerum isolate (HQ647302)99KP018374
Sm-1-5-3Macrophoma sp. TXc4-6 (HQ262514)100KP018375
Sm-1-6-2Alternaria sp. BJ35 (KJ702610)100KP018376
Sm-1-9-2-2Macrophoma sp. TXc4-6 (HQ262514)100KP018377
Sm-1-10-1Fusarium andiyazi strain CBS 134430 (KC954400)100KP018378
Sm-1-10-2Alternaria sp. BJ35 (KJ702610)100KP018379
Sm-2-1-3Alternaria sp. BJ35 (KJ702610)100KP018380
Sm-2-6-1Macrophoma sp. TXc4-6 (HQ262514)100KP018381
Sm-2-6-2Alternaria sp. BJ35 (KJ702610)100KP018382
Sm-2-7-2Macrophoma sp. TXc4-6 (HQ262514)100KP018383
Sm-2-8-1Talaromyces trachyspermus strain (KF147920)99KP018384
Sm-2-8-2-1Exophiala oligosperma (AB777520)100KP018385
Sm-2-8-2-2Meira sp. JCM 18504 (AB778892)99KP018386
Sm-2-9-1Alternaria sp. DX-FOF7 (KF558883)100KP018387
Sm-2-9-2Alternaria sp. BJ35 (KJ702610)100KP018388
Sm-2-10-1Alternaria sp. HT-M18-LS (KJ527010)100KP018389
Sm-2-10-2Cladosporium cladosporioides strain (KJ589558)100KP018390
Sm-3-1-1Macrophoma sp. TXc4-6 (HQ262514)99KP018391
Sm-3-1-3Cladosporium oxysporum strain B2F2 (KJ589590)100KP018392
Sm-3-2-1Alternaria sp. BJ35 (KJ702610)100KP018393
Sm-3-3-3Penicillium sp. JMG302 (KJ598874)98KP018394
Sm-3-4-1Cochliobolus kusanoi isolate SH8 (KJ572135)100KP018395
Sm-3-5-1Alternaria sp. DX-FOF7 (KF558883)100KP018396
Sm-3-8-1Alternaria sp. DX-FOF7 (KF558883)100KP018397
Sm-3-8-2Macrophoma sp. TXc4-6 (HQ262514)100KP018398
Sm-3-9-2Macrophoma sp. TXc4-6 (HQ262514)100KP018399
Sm-3-10-2Alternaria sp. HT-M18-LS (KJ527010)100KP018400
Sm-3-10-3Cladosporium cladosporioides strain (KJ589558)100KP018401


Table 3 . Endophytic fungi (188 strains) isolated from five plants with scientific names, plant codes, taxa of fungal strain, and number of fungal isolates..

Scientific name of plant sampleAbbreviated plant nameTaxon of fungal strainsNo. of isolates
Phragmites australisPa14 genera, 16 species52
Suaeda australisSa17 genera, 17 species40
Limonium tetragonumLt14 genera, 13 species25
Suaeda glauca BungeSu19 genera, 14 species41
Suaeda maritimaSm11 genera, 7 species30

Pa, Phragmites australis; Sa, Suaeda australis; Lt, Limonium tetragonum; Su, Suaeda glauca Bunge; and Sm, Suaeda maritima..


Table 4 . Diversity indices and distribution of endophytic fungi isolated from plants native to the Buan salt marsh..

Fungal taxonPaSaLtSuSm
Acrostalagmus2
Alternaria1034611
Aspergillus4231
Cladosporium3113
Clonostachys1
Cochliobolus11
Colletotrichum112
Davidiella2
Exophiala21
Fusarium145221
Gibberella1
Gliomastix1
Hypocrea11
Lecanicillium1
Lewia71
Macrophoma18118
Meira11
Metacordyceps1
Paraconiothyrium11
Paraphoma1
Penicillium45441
Pestalotiopsis122
Phoma3211
Phomopsis2
Plectosphaerella1
Pleospora125
Purpureocillium3
Sclerostagonospora11
Simplicillium1
Talaromyces221
Tetracladium1
Trichoderma212
Verticillium2
N5240254130
S1417141911
Shannon diversity index (H')2.222.552.502.761.86
Simpson’s index of diversity (1-D)0.9040.9360.9670.9700.929
Menhinick's index (Dmn)1.942.692.802.972.01
Margalef's index (Dmg)3.294.344.044.852.94
Fisher's diversity (α)6.2911.1713.1413.756.26

Pa, Phragmites australis; Sa, Suaeda australis; Lt, Limonium tetragonum; Su, Suaeda glauca Bunge; and Sm, Suaeda maritima..


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