The first report of dark septate endophytes from Indonesian Pinus merkusii and its symbiosis role as a plant growth promoter in nursery condition

##plugins.themes.bootstrap3.article.main##

JUMADIL AKHIR
ELIS NINA HERLIYANA
SURONO
SRI WILARSO BUDI

Abstract

Abstract. Akhir J, Herliyana EN, Surono, Budi SW. 2024. The first report of dark septate endophytes from Indonesian Pinus merkusii and its symbiosis role as a plant growth promoter in nursery condition. Biodiversitas 25: 312-321. To encourage the healthy growth of Pinus merkusii Jungh et de Vriese seedlings at the seedling stage, Dark Septate Endophytic (DSE) fungi were used as growth promoters. In this study, four DSE strains, i.e., Apls 1.5.3, Pls 32.1, Hs14.6a, and Hs14.6c isolated from P. merkusii roots, were tested for their ability to stimulate the growth of P. merkusii seedlings. After 14 weeks of incubation in nursery conditions, P. merkusii seedlings inoculated with four DSE strains experienced a higher increase in height and stem diameter when compared to the control treatment. Overall, the biomass results of P. merkusii seedlings treated with the DSE strains performed better than those of the control. Root colonization of P. merkusii seedlings showed that the 4 DSE strains significantly outperformed the control. The Hs14.6c strain outperformed the other strains and controls regarding nutrient (nitrogen) uptake. The findings of this study are the first to show that the DSE Apls 1.5.3 strain is similar to Cylindroccarpon, the Hs14.6a and Hs14.6c strains are similar to Cladophialophora sp., and the Pls 32.1 strain is similar to Oncopodiella trigonella based on identification results and phylogenetic trees and can be in symbiosis with seeds of P. merkusii, a pine species native to Indonesia.

##plugins.themes.bootstrap3.article.details##

References
Adhikari TB, Hodges CS, Louws FJ (2013) First report of Cylindrocarpon sp. Associated with root rot disease of strawberry in North Carolina. Plant Dis 97:1251. DOI: 10.1094/PDIS-01-13-0116-PDN
Aigoun-Mouhous W, Elena G, Cabral A, et al (2019) Characterization and pathogenicity of Cylindrocarpon-like asexual morphs associated with black foot disease in Algerian grapevine nurseries, with the description of Pleiocarpon algeriense sp. nov. Eur J Plant Pathol 154:887–901. DOI: 10.1007/s10658-019-01708-z
Alberton O, Kuyper TW, Summerbell RC (2010) Dark septate root endophytic fungi increase growth of Scots pine seedlings under elevated CO2 through enhanced nitrogen use efficiency. Plant Soil 328:459–470. DOI: 10.1007/s11104-009-0125-8
Almario J, Jeena G, Wunder J, et al (2017) Root-associated fungal microbiota of nonmycorrhizal Arabis alpina and its contribution to plant phosphorus nutrition. Proc Natl Acad Sci U S A 114:E9403–E9412. DOI: 10.1073/pnas.1710455114
Backman PA, Sikora RA (2008) Endophytes: An emerging tool for biological control. Biol Control 46:1–3. DOI: 10.1016/j.biocontrol.2008.03.009
Beltran-Garcia MJ, Martínez-Rodríguez A, Olmos-Arriaga I, et al (2021) Nitrogen fertilization and stress factors drive shifts in microbial diversity in soils and plants. Symbiosis 84:379–390. DOI: 10.1007/s13199-021-00787-z
Capote N, Del Río MÁ, Herencia JF, Arroyo FT (2022) Molecular and Pathogenic Characterization of Cylindrocarpon-like Anamorphs Causing Root and Basal Rot of Almonds. Plants 11:984. DOI: 10.3390/plants11070984
Carpenter CL, White M, Serpe MD (2021) Co-inoculation with a dark septate endophyte alters arbuscular mycorrhizal colonization of two widespread plants of the sagebrush steppe. Symbiosis 85:343–357. DOI: 10.1007/s13199-021-00819-8
Chu H, Wang C, Li Z, et al (2019) The dark septate endophytes and ectomycorrhizal fungi effect on Pinus tabulaeformis Carr. Seedling growth and their potential effects to pine wilt disease resistance. Forests 10:140. DOI: 10.3390/f10020140
Deng X, Song X, Halifu S, et al (2020) Effects of dark septate endophytes strain A024 on damping-off biocontrol, plant growth and the rhizosphere soil enviroment of Pinus sylvestris var. Mongolica annual seedlings. Plants 9:1–19. DOI: 10.3390/plants9070913
Dhyani A, Jain R, Pandey A (2019) Contribution of root-associated microbial communities on soil quality of Oak and Pine forests in the Himalayan ecosystem. Trop Ecol 60:271–280. DOI: 10.1007/s42965-019-00031-2
Doty SL (2011) Growth-Promoting Endophytic Fungi of Forest Trees. In: Endophytes of forest trees: biology and applications. Springer, pp 151–156. DOI: 10.1007/978-94-007-1599-8_9
Etesami H, Adl SM (2020) Plant Growth-Promoting Rhizobacteria (PGPR) and Their Action Mechanisms in Availability of Nutrients to Plants. In: Phyto-microbiome in stress regulation. Springer, pp 147–203. DOI: 10.1007/978-981-15-2576-6_9
Farjon A (2021) Pines: Drawings and Descriptions of the Genus, Pinus. Brill
Fontana DC, de Paula S, Torres AG, et al (2021) Endophytic fungi: Biological control and induced resistance to phytopathogens and abiotic stresses. Pathogens 10:570. DOI: 10.3390/pathogens10050570
Hadiyane A, Sulistyawati E, Asharina WP, Dungani R (2015) A study on production of resin from pinus merkusii jungh. Et De vriese in the Bosscha observatory area, west Java-Indonesia. Asian J Plant Sci 14:89–93. DOI: 10.3923/ajps.2015.89.93
Han JH, Park GC, Kim KS (2017) Antagonistic evaluation of Chromobacterium sp. JH7 for biological control of ginseng root rot caused by Cylindrocarpon destructans. Mycobiology 45:370–378. DOI: 10.5941/MYCO.2017.45.4.370
Harsonowati W, Marian M, Surono M, Narisawa K (2020) The Effectiveness of a Dark Septate Endophytic Fungus, Cladophialophora chaetospira SK51, to Mitigate Strawberry Fusarium Wilt Disease and With Growth Promotion Activities. Front Microbiol 11:585. DOI: 10.3389/fmicb.2020.00585
Hartiningtias D, Fulé PZ, Gunawan AA (2020) Wildfire effects on forest structure of Pinus merkusii in Sumatra, Indonesia. For Ecol Manage 457:117660. DOI: 10.1016/j.foreco.2019.117660
He C, Wang W, Hou J (2019) Characterization of dark septate endophytic fungi and improve the performance of liquorice under organic residue treatment. Front Microbiol 10:1364. DOI: 10.3389/fmicb.2019.01364
Hernández-Restrepo M, Gené J, Castañeda-Ruiz RF, et al (2017) Phylogeny of saprobic microfungi from Southern Europe. Stud Mycol 86:53–97. DOI: 10.1016/j.simyco.2017.05.002
Hiruma K, Gerlach N, Sacristán S, et al (2016) Root Endophyte Colletotrichum tofieldiae Confers Plant Fitness Benefits that Are Phosphate Status Dependent. Cell 165:464–474. DOI: 10.1016/j.cell.2016.02.028
Hou L, Yu J, Zhao L, He X (2020) Dark Septate Endophytes Improve the Growth and the Tolerance of Medicago sativa and Ammopiptanthus mongolicus Under Cadmium Stress. Front Microbiol 10:3061. DOI: 10.3389/fmicb.2019.03061
Imanuddin R, Hidayat A, Rachmat HH, et al (2020) Reforestation and sustainable management of pinus merkusii forest plantation in indonesia: A review. Forests 11:1–22. DOI: 10.3390/f11121235
Kageyama SA, Mandyam KG, Jumpponen A (2008) Diversity, function and potential applications of the root-associated endophytes. Mycorrhiza State Art, Genet Mol Biol Eco-Function, Biotechnol Eco-Physiology, Struct Syst (Third Ed 29–57. DOI: 10.1007/978-3-540-78826-3_2
Kamdem RST, Pascal W, Rehberg N, et al (2018) Metabolites from the endophytic fungus Cylindrocarpon sp. isolated from tropical plant Sapium ellipticum. Fitoterapia 128:175–179. DOI: 10.1016/j.fitote.2018.05.020
Kormanik PP, Bryan WC, Schultz RC (1980) Procedures and equipment for staining large numbers of plant root samples for endomycorrrhizal assay. Can J Microbiol 26:536–538. DOI: 10.1139/m80-090
Kumar S, Yadav AK, Chambel P, Kaur R (2017) Molecular and functional characterization of myxobacteria isolated from soil in India. 3 Biotech 7:1–9. DOI: 10.1007/s13205-017-0722-9
Lavallee JM, Soong JL, Cotrufo MF (2020) Conceptualizing soil organic matter into particulate and mineral-associated forms to address global change in the 21st century. Glob Chang Biol 26:261–273. DOI: 10.1111/gcb.14859
Lawrence DP, Nouri MT, Trouillas FP (2019) Taxonomy and multi-locus phylogeny of cylindrocarpon-like species associated with diseased roots of grapevine and other fruit and nut crops in California. Fungal Syst Evol 4:59–75. DOI: 10.3114/fuse.2019.04.06
Li X, He C, He X, et al (2019) Dark septate endophytes improve the growth of host and non-host plants under drought stress through altered root development. Plant Soil 439:259–272. DOI: 10.1007/s11104-019-04057-2
Liu H, Li T, Ding Y, et al (2017) Dark septate endophytes colonizing the roots of ‘non-mycorrhizal’ plants in a mine tailing pond and in a relatively undisturbed environment, Southwest China. J Plant Interact 12:264–271. DOI: 10.1080/17429145.2017.1333635
Magyar D, Révay Á (2009) New species of oncopodiella (hyphomycetes) from living trees. Nov Hedwigia 88:169–182. DOI: 10.1127/0029-5035/2009/0088-0169
Mandyam K, Jumpponen A (2014) Seeking the elusive function of the root-colonising dark septate endophytic fungi. Stud Mycol 79:221–288. DOI: 10.3114/sim.53.1.173
Miransari M (2013) Soil microbes and the availability of soil nutrients. Acta Physiol Plant 35:3075–3084. DOI: 10.1007/s11738-013-1338-2
Nascimento SS, Ferro LO, Freire KTLS, et al (2021) Cladophialophora bromeliacearum (Herpotrichiellaceae, Chaetothyriales), a novel endophytic species from the Brazilian tropical dry forest. Phytotaxa 509:211–224. DOI: 10.11646/phytotaxa.509.2.4
Obase K, Matsuda Y (2014) Culturable fungal endophytes in roots of Enkianthus campanulatus (Ericaceae). Mycorrhiza 24:635–644. DOI: 10.1007/s00572-014-0584-5
Park MJ, Shin HD (2011) Cladophialophora pucciniophila, a new hyphomycete parasitizing a rust fungus. Mycotaxon 116:449–456. DOI: 10.5248/116.449
Poveda J, Eugui D, Abril-Urías P, Velasco P (2021) Endophytic fungi as direct plant growth promoters for sustainable agricultural production. Symbiosis 85:1–19. DOI: 10.1007/s13199-021-00789-x
Punja ZK, Ni L, Roberts A (2021) The Fusarium solani species complex infecting cannabis (Cannabis sativa L., marijuana) plants and a first report of Fusarium (Cylindrocarpon) lichenicola causing root and crown rot. Can J Plant Pathol 43:567–581. DOI: 10.1080/07060661.2020.1866672
Purba PR, Rahmawaty, Susilowati A (2022) Analysis of income from pine resin tapping on Forest Farmers Groups in partnership with UPT KPH Region II Pematang Siantar. In: IOP Conference Series: Earth and Environmental Science. p 12060. DOI: 10.1088/1755-1315/1115/1/012060
Richardson DM, Rundel PW, Jackson ST, et al (2007) Human impacts in pine forests: past, present, and future. Annu Rev Ecol Evol Syst 38:275–297. DOI: 10.1146/annurev.ecolsys.38.091206.095650
Santos M, Cesanelli I, Diánez F, et al (2021) Advances in the role of dark septate endophytes in the plant resistance to abiotic and biotic stresses. J Fungi 7:939. DOI: 10.3390/jof7110939
Schroers HJ, Žerjav M, Munda A, et al (2008) Cylindrocarpon pauciseptatum sp. nov., with notes on Cylindrocarpon species with wide, predominantly 3-septate macroconidia. Mycol Res 112:82–92. DOI: 10.1016/j.mycres.2007.10.004
Sharma H, Rai AK, Dahiya D, et al (2021) Exploring endophytes for in vitro synthesis of bioactive compounds similar to metabolites produced in vivo by host plants. AIMS Microbiol 7:175–199. DOI: 10.3934/MICROBIOL.2021012
Silva NM da, Reis GF, Costa F de F, et al (2023) Genome sequencing of Cladophialophora exuberans, a novel candidate for bioremediation of hydrocarbon and heavy metal polluted habitats. Fungal Biol 127:1032–1042. DOI: 10.1016/j.funbio.2023.03.003
Stambaugh MC, Guyette RP, Marschall JM (2011) Longleaf pine (Pinus palustris Mill.) fire scars reveal new details of a frequent fire regime. J Veg Sci 22:1094–1104. DOI: 10.1111/j.1654-1103.2011.01322.x
Surono, Narisawa K (2018) The inhibitory role of dark septate endophytic fungus Phialocephala fortinii against Fusarium disease on the Asparagus officinalis growth in organic source conditions. Biol Control 121:159–167. DOI: 10.1016/j.biocontrol.2018.02.017
Surono, Narisawa K (2017) The dark septate endophytic fungus Phialocephala fortinii is a potential decomposer of soil organic compounds and a promoter of Asparagus officinalis growth. Fungal Ecol 28:1–10. DOI: 10.1016/j.funeco.2017.04.001
Suzuki T, Yoshida S, Koseki T, et al (2018) New Metabolites Produced by Cylindrocarpon sp. SY-39 from a Driftwood. Chem Biodivers 15:e1700493. DOI: 10.1002/cbdv.201700493
Tamura K, Stecher G, Peterson D, et al (2013) MEGA6: Molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729. DOI: 10.1093/molbev/mst197
Tienaho J, Karonen M, Muilu--Mäkelä R, et al (2019) Metabolic profiling of water-soluble compounds from the extracts of dark septate endophytic fungi (DSE) isolated from scots pine (Pinus sylvestris L.) seedlings using UPLC--Orbitrap--MS. Molecules 24:2330. DOI: 10.3390/molecules24122330
Wagg C, Pautler M, Massicotte HB, Peterson RL (2008) The co-occurrence of ectomycorrhizal, arbuscular mycorrhizal, and dark septate fungi in seedlings of four members of the Pinaceae. Mycorrhiza 18:103–110. DOI: 10.1007/s00572-007-0157-y
Wang S, Bi Y, Quan W, Christie P (2022) Growth and metabolism of dark septate endophytes and their stimulatory effects on plant growth. Fungal Biol 126:674–686. DOI: 10.1016/j.funbio.2022.08.006
Xie L, Bi Y, Ma S, et al (2021) Combined inoculation with dark septate endophytes and arbuscular mycorrhizal fungi: synergistic or competitive growth effects on maize? BMC Plant Biol 21:1–11. DOI: 10.1186/s12870-021-03267-0
Yihui BAN, Zhouying XU, Yurong Y, et al (2017) Effect of dark septate endophytic fungus Gaeumannomyces cylindrosporus on plant growth, photosynthesis and Pb tolerance of maize (Zea mays L.). Pedosphere 27:283–292. DOI: 10.1016/S1002-0160(17)60316-3
Yoshida S, Suzuki T, Furuno H, et al (2018) Spectroscopic characterisation of two polyketide metabolites from Cylindrocarpon sp. from driftwood. Nat Prod Res 32:60–64. DOI: 10.1080/14786419.2017.1332616.

Most read articles by the same author(s)