Dark Septate Endophytes: Important Partners of Mycorrhizal Fungi and Their Genomic Signatures for Adaptation

LI Zhongfeng, ZHU Zhiyong, YUAN Zhilin

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Bulletin of Botanical Research ›› 2025, Vol. 45 ›› Issue (03) : 352-360. DOI: 10.7525/j.issn.1673-5102.2025.03.006
Review Article

Dark Septate Endophytes: Important Partners of Mycorrhizal Fungi and Their Genomic Signatures for Adaptation

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Abstract

Dark septate endophytes（DSEs） constitute an important component of root-associated mycobiome and typically develop microsclerotia-like structures in cortical cells. Generally， DSEs perform functions similar to those of mycorrhizal fungi in promoting plant growth， nutrient uptake and stress tolerance. Under certain extreme environments， the abundance of DSEs often exceeds that of mycorrhizal fungi. In this review article， we first summarized the species diversity， basic biological traits and eco-physiological functions played by DSEs， an important component of root-associated mycobiome. We then mainly focused on the advances concerning mechanisms underlying plant-DSEs mutualism as well as genomic signatures and evolutionary adaptation of DSEs. Together， our understanding of more adaptive potentials of DSEs and their extended effects on improving plant abiotic tolerance emerged. Promisingly， the development of robust DSE inoculants used for ecological restoration of soils and improvement of plant productivity in agro-forestry systems under stressful environment was briefly discussed.

Key words

dark septate endophytes / mycorrhizal fungi / mutualistic relationships / population divergence

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LI Zhongfeng , ZHU Zhiyong , YUAN Zhilin. Dark Septate Endophytes: Important Partners of Mycorrhizal Fungi and Their Genomic Signatures for Adaptation. Bulletin of Botanical Research. 2025, 45(03): 352-360 https://doi.org/10.7525/j.issn.1673-5102.2025.03.006

References

List( Publishing order | Descend order by publishing year | Descend order by cited within ) Chart analysis
1
FIELD K J， PRESSEL S， DUCKETT J G，et al.Symbiotic options for the conquest of land［J］.Trends in Ecology & Evolution，2015，30（8）：477-486.
本文引用 [1]
2
NETHERWAY T， BENGTSSON J， BUEGGER F，et al.Pervasive associations between dark septate endophytic fungi with tree root and soil microbiomes across Europe［J］.Nature Communications，2024，15（1）：159.
本文引用 [4]
3
SMITH S E， READ D.Mycorrhizal symbiosis［M］.3rd ed.New York：Academic Press，2008.
本文引用 [1]
4
RODRIGUEZ R J， WHITE Jr J F， ARNOLD A E，et al.Fungal endophytes：diversity and functional roles［J］.New Phytologist，2009，182（2）：314-330.
本文引用 [2]
5
MARTIN F M， UROZ S， BARKER D G.Ancestral alliances：plant mutualistic symbioses with fungi and bacteria［J］.Science，2017，356（6340）：eaad4501.
6
KARIMAN K， BARKER S J， TIBBETT M.Structural plasticity in root-fungal symbioses：diverse interactions lead to improved plant fitness［J］.PeerJ，2018，6：e6030.
本文引用 [1]
7
MELIN E.On the mycorrhizas of Pinus Silvestris L. and Picea abies Karst：a preliminary note［J］.Journal of Ecology，1922，9（2）：254-257.
本文引用 [1]
8
JUMPPONEN A， TRAPPE J M.Dark septate endophytes：a review of facultative biotrophic root-colonizing fungi［J］.New Phytologist，1998，140（2）：295-310.
本文引用 [1]
9
KNAPP D G， KOVÁCS G M， ZAJTA E，et al.Dark septate endophytic pleosporalean genera from semiarid areas［J］.Persoonia，2015，35：87-100.
本文引用 [2]
10
HILL P W， BROUGHTON R， BOUGOURE J，et al.Angiosperm symbioses with non-mycorrhizal fungal partners enhance N acquisition from ancient organic matter in a warming maritime Antarctic［J］.Ecology Letters，2019，22（12）：2111-2119.
本文引用 [1]
11
MATEU M G， BALDWIN A H， MAUL J E，et al.Dark septate endophyte improves salt tolerance of native and invasive lineages of Phragmites australis ［J］.The ISME Journal，2020，14（8）：1943-1954.
12
HAN L， ZUO Y L， HE X L，et al.Plant identity and soil variables shift the colonisation and species composition of dark septate endophytes associated with medicinal plants in a northern farmland in China［J］.Applied Soil Ecology，2021，167：104042.
本文引用 [1]
13
SANTOS M， CESANELLI I， DIÁNEZ F，et al.Advances in the role of dark septate endophytes in the plant resistance to abiotic and biotic stresses［J］.Journal of Fungi，2021，7（11）：939.
本文引用 [1]
14
SIEBER T N.Fungal root endophytes［M］//WAISEL Y，ESHEL A，KAFKAI U.Plant roots：the hidden half.New York：Marcel Dekker，2002：887-917.
本文引用 [1]
15
MALICKA M， MAGURNO F， PIOTROWSKA-SEGET Z.Plant association with dark septate endophytes：when the going gets tough（and stressful），the tough fungi get going［J］.Chemosphere，2022，302：134830.
本文引用 [1]
16
YUAN Z L， LIN F C， ZHANG C L，et al.A new species of Harpophora（Magnaporthaceae） recovered from healthy wild rice（Oryza granulata） roots，representing a novel member of a beneficial dark septate endophyte［J］.FEMS Microbiology Letters，2010，307（1）：94-101.
本文引用 [1]
17
WEI H S， HE X H， RICCARDO B，et al. Stagonosporopsis rhizophilae sp.nov.（Didymellaceae，Pleosporales），a new rhizospheric soil fungus associated with Populus deltoides Marsh［J］.Phytotaxa，2021，491：23-34.
本文引用 [1]
18
WEI X H， LONG Y Y， CHEN Y L，et al. Cladophialophora guangxiense sp.nov.，a new species of dark septate endophyte，mitigates tomato bacterial wilt and growth promotion activities［J］.Agronomy，2024，14（12）：2771.
本文引用 [1]
19
YUAN Z L， DRUZHININA I S， WANG X Y，et al.Insight into a highly polymorphic endophyte isolated from the roots of the halophytic seepweed Suaeda salsa：Laburnicola rhizohalophila sp.nov.（Didymosphaeriaceae，Pleosporales）［J］.Fungal Biology，2020，124（5）：327-337.
本文引用 [1]
20
ASHRAFI S， WENNRICH J P， BECKER Y，et al. Polydomus karssenii gen.nov.sp.nov.is a dark septate endophyte with a bifunctional lifestyle parasitising eggs of plant parasitic cyst nematodes（Heterodera spp.）［J］.IMA Fungus，2023，14（1）：6.
本文引用 [1]
21
GRÜNIG C R， SIEBER T N.Molecular and phenotypic description of the widespread root symbiont Acephala applanata gen.et sp.nov.，formerly known as dark-septate endophyte type 1［J］.Mycologia，2005，97（3）：628-640.
本文引用 [1]
22
GRÜNIG C R， QUELOZ V， DUÒ A，et al.Phylogeny of Phaeomollisia piceae gen.sp.nov.：a dark，septate，conifer-needle endophyte and its relationships to Phialocephala and Acephala ［J］.Mycological Research，2009，113（2）：207-221.
23
WALSH E， LUO J， ZHANG N. Acidomelania panicicola gen.et sp.nov.from switchgrass roots in acidic New Jersey pine barrens［J］.Mycologia，2014，106（4）：856-864.
24
WALSH E， LUO J， NAIK A，et al. Barrenia，a new genus associated with roots of switchgrass and pine in the oligotrophic pine barrens［J］.Fungal Biology，2015，119（12）：1216-1225.
25
VOHNÍK M， BOROVEC O， KOLAŘÍKOVÁ Z，et al.Extensive sampling and high-throughput sequencing reveal Posidoniomyces atricolor gen.et sp.nov.（Aigialaceae，Pleosporales） as the dominant root mycobiont of the dominant Mediterranean seagrass Posidonia oceanica ［J］.MycoKeys，2019，55：59-86.
26
LONG Y Y， NONG Q， XIE L，et al. Tiankengomelania guangxiense，gen.et sp.nov.，a dark septate endophytic fungus，promotes the growth of the medicinal orchid Dendrobium officinale ［J］.Fungal Biology，2022，126（5）：333-341.
27
IMREFI I， KNAPP D G， KOVÁCS G M. Poaceascoma zborayi sp.nov.and Agrorhizomyces patris gen.et spec.nov.：two novel dark septate endophytes colonizing wheat（Triticum aestivum） roots from a cropland in Hungary［J］.Mycological Progress，2024，23（1）：35.
本文引用 [1]
28
DE MESQUITA C P B， SARTWELL S A， ORDEMANN E V，et al.Patterns of root colonization by arbuscular mycorrhizal fungi and dark septate endophytes across a mostly-unvegetated，high-elevation landscape［J］.Fungal Ecology，2018，36：63-74.
本文引用 [1]
29
STEIDINGER B S， CROWTHER T W， LIANG J，et al.Climatic controls of decomposition drive the global biogeography of forest-tree symbioses［J］.Nature，2019， 569（7756）：404-408.
本文引用 [1]
30
LOPEZ R O， CHIOCCHIO V M， RUSCITTI M F，et al.Towards a better understanding of melanins from dark septate endophytes（DSEs）：their variability，synthesis pathways and biological roles［J］.Journal of Soil Science and Plant Nutrition，2024，24：1650-1664.
本文引用 [3]
31
杜金茹，王守现，严冬，等.基于全基因组数据分析香菇黑色素合成途径及相关基因［J］.菌物学报，2023，42（5）：1114-1128.
DU J R， WANG S X， YAN D，et al.Analyses of melanin synthesis pathway and the related genes in Lentinula edodes based on whole genome sequence comparison［J］.Mycosystema，2023，42（5）：1114-1128.
本文引用 [1]
32
ZHAN F D， HE Y M， ZU Y Q，et al.Characterization of melanin isolated from a dark septate endophyte（DSE），Exophiala pisciphila ［J］.World Journal of Microbiology and Biotechnology，2011，27：2483-2489.
本文引用 [1]
33
LI X， HE C， HE X L，et al.Dark septate endophytes improve the growth of host and non-host plants under drought stress through altered root development［J］.Plant and Soil，2019，439：259-272.
34
POTISEK M， LIKAR M， VOGEL-MIKUŠ K，et al.1，8-dihydroxy naphthalene（DHN）-melanin confers tolerance to cadmium in isolates of melanised dark septate endophytes［J］.Ecotoxicology and Environmental Safety，2021，222：112493.
本文引用 [1]
35
RUOTSALAINEN A L， MARKKOLA A， KOZLOV M V.Root fungal colonisation in Deschampsia flexuosa：effects of pollution and neighbouring trees［J］.Environmental Pollution，2007，147（3）：723-728.
本文引用 [1]
36
BAN Y H， TANG M， CHEN H，et al.The response of dark septate endophytes（DSE） to heavy metals in pure culture［J］.PLoS One，2012，7（10）：e47968.
37
赵之伟，李涛.重金属矿区深色有隔内生真菌资源及其生态学功能［J］.中国科学：生命科学，2019，49（7）：921-926.
ZHAO Z W， LI T.Dark septate endophytes and their ecological function in metal mining areas［J］.Scientia Sinica（Vitae），2019，49（7）：921-926.
本文引用 [1]
38
WEI H S， ZHONG Z H， LI Z F，et al.Loss of the accessory chromosome converts a pathogenic tree-root fungus into a mutualistic endophyte［J］.Plant Communications，2024，5（1）：100672.
本文引用 [5]
39
MARTIN F， KOHLER A， MURAT C，et al.Unearthing the roots of ectomycorrhizal symbioses［J］.Nature Reviews Microbiology，2016，14（12）：760-773.
本文引用 [1]
40
PEROTTO S， DAGHINO S， MARTINO E.Ericoid mycorrhizal fungi and their genomes：another side to the mycorrhizal symbiosis？［J］.New Phytologist，2018，220（4）：1141-1147.
本文引用 [1]
41
KNAPP D G， NÉMETH J B， BARRY K，et al.Comparative genomics provides insights into the lifestyle and reveals functional heterogeneity of dark septate endophytic fungi［J］.Scientific Reports，2018，8（1）：6321.
本文引用 [1]
42
HE X H， YUAN Z L.Near-chromosome-level genome assembly of the dark septate endophyte Laburnicola rhizohalophila：a model for investigating root-fungus symbiosis［J］.Genome Biology and Evolution，2021，13（3）：evab026.
本文引用 [1]
43
RUOTSALAINEN A L， KAUPPINEN M， WÄLI P R，et al.Dark septate endophytes：mutualism from by-products？［J］.Trends in Plant Science，2022，27（3）：247-254.
本文引用 [1]
44
LUKEŠOVÁ T， KOHOUT P， VĚTROVSKÝ T，et al.The potential of dark septate endophytes to form root symbioses with ectomycorrhizal and ericoid mycorrhizal middle European forest plants［J］.PLoS One，2015，10（4）：e0124752.
本文引用 [1]
45
ALMARIO J， FABIAŃSKA I， SARIDIS G，et al.Unearthing the plant-microbe quid pro quo in root associations with beneficial fungi［J］.New Phytologist，2022，234（6）：1967-1976.
本文引用 [1]
46
CALDWELL B A， JUMPPONEN A， TRAPPE J M.Utilization of major detrital substrates by dark-septate，root endophytes［J］.Mycologia，2000，92（2）：230-232.
本文引用 [2]
47
NEWSHAM K K.A meta-analysis of plant responses to dark septate root endophytes［J］.New Phytologist，2011，190（3）：783-793.
本文引用 [2]
48
PENG L， ZHANG Y， DRUZHININA I S，et al.A facultative ectomycorrhizal association is triggered by organic nitrogen［J］.Current Biology，2022，32（24）：5235-5249.
本文引用 [1]
49
ROBERTS P， NEWSHAM K K， BARDGETT R D，et al.Vegetation cover regulates the quantity，quality and temporal dynamics of dissolved organic carbon and nitrogen in Antarctic soils［J］.Polar Biology，2009，32：999-1008.
本文引用 [1]
50
毕银丽，宋雅宁，白雪蕊，等.AMF和DSE对紫花苜蓿生长发育及叶片代谢组分的影响［J］.菌物学报，2024，43（5）：230209.
BI Y L， SONG Y N， BAI X R，et al.Effects of AMF and DSE on the growth and development and metabolic fractions of leaves of Medicago sativa ［J］.Mycosystema，2024，43（5）：230209.
本文引用 [1]
51
XIE L L， BI Y L， MA S P，et al.Combined inoculation with dark septate endophytes and arbuscular mycorrhizal fungi：synergistic or competitive growth effects on maize？［J］.BMC Plant Biology，2021，21（1）：498.
本文引用 [1]
52
GUO X L， WANG Y Q， HU J B，et al.Mixed inoculation of dark septate endophytic and ericoid mycorrhizal fungi in different proportions improves the growth and nutrient content of blueberry seedlings［J］.Plant Biosystems，2023，157（3）：497-506.
本文引用 [1]
53
DELLA MÓNICA I F， SAPARRAT M C N， GODEAS A M，et al.The co-existence between DSE and AMF symbionts affects plant P pools through P mineralization and solubilization processes［J］.Fungal Ecology，2015，17：10-17.
本文引用 [1]
54
WANG Z D， WANG L， LIANG X R，et al.The coexistence of arbuscular mycorrhizal fungi and dark septate endophytes synergistically enhanced the cadmium tolerance of maize［J］.Frontiers in Plant Science，2024，15：1349202.
本文引用 [1]
55
ZHOU Y， ZHENG Y Y， LI P W，et al.Ectomycorrhizal fungi and dark septate endophyte inoculation improve growth and tolerance of Pinus tabulaeformis under cadmium stress［J］.Pedosphere，2024，34（2）：473-483.
本文引用 [1]
56
CHU H L， WANG H H， ZHANG Y N，et al.Inoculation with ectomycorrhizal fungi and dark septate endophytes contributes to the resistance of Pinus spp. to pine wilt disease［J］.Frontiers in Microbiology，2021，12：687304.
本文引用 [1]
57
BI Y L， XIE L L， WANG X，et al.Phosphorus reward mechanisms of arbuscular mycorrhizal fungi and dark septate endophytes：synergism or competition in plant carbon allocation？［J/OL］.Pedosphere，（2024-05-20）［2024-12-26］.
https://doi.org/10.1016/j.pedsph.2024. 05.010
本文引用 [1]
58
BAHRAM M， PÕLME S， KÕLJALG U，et al.A single European aspen（Populus tremula） tree individual may potentially harbour dozens of Cenococcum geophilum ITS genotypes and hundreds of species of ectomycorrhizal fungi［J］.FEMS Microbiology Ecology，2011，75（2）：313-320.
本文引用 [2]
59
DAUPHIN B， DE FREITAS PEREIRA M， KOHLER A，et al.Cryptic genetic structure and copy-number variation in the ubiquitous forest symbiotic fungus Cenococcum geophilum ［J］.Environmental Microbiology，2021，23（11）：6536-6556.
本文引用 [2]
60
JOHNSON D， MARTIN F， CAIRNEY J W G，et al.The importance of individuals：intraspecific diversity of mycorrhizal plants and fungi in ecosystems［J］.New Phytologist，2012，194（3）：614-628.
本文引用 [1]
61
WYSS T， MASCLAUX F G， ROSIKIEWICZ P，et al.Population genomics reveals that within-fungus polymorphism is common and maintained in populations of the mycorrhizal fungus Rhizophagus irregularis ［J］.The ISME Journal，2016，10（10）：2514-2526.
本文引用 [1]
62
BRANCO S， GLADIEUX P， ELLISON C E，et al.Genetic isolation between two recently diverged populations of a symbiotic fungus［J］.Molecular Ecology，2015，24（11）：2747-2758.
本文引用 [1]
63
GLYNOU K，ALI T， KIA S H，et al.Genotypic diversity in root-endophytic fungi reflects efficient dispersal and environmental adaptation［J］.Molecular Ecology，2017，26（18）：4618-4630.
本文引用 [1]
64
YUAN Z L， DRUZHININA I S， GIBBONS J G，et al.Divergence of a genomic island leads to the evolution of melanization in a halophyte root fungus［J］.The ISME Journal，2021，15（12）：3468-3479.
本文引用 [1]
65
CAMPBELL M A， TAPPER B A， SIMPSON W R，et al. Epichloë hybrida，sp.nov.，an emerging model system for investigating fungal allopolyploidy［J］.Mycologia，2017，109（5）：715-729.
本文引用 [1]
66
LI Z F， ZHU Z Y， QIAN K，et al.Intraspecific diploidization of a halophyte root fungus drives heterosis［J］.Nature Communications，2024，15（1）：5872.
本文引用 [1]
67
ORCHARD S， STANDISH R J， DICKIE I A，et al.Fine root endophytes under scrutiny：a review of the literature on arbuscule-producing fungi recently suggested to belong to the Mucoromycotina［J］.Mycorrhiza，2017， 27（7）：619-638.
本文引用 [1]
68
PROUT J N， WILLIAMS A， WANKE A，et al.Mucoromycotina ‘fine root endophytes’：a new molecular model for plant-fungal mutualisms？［J］.Trends in Plant Science，2024，29（6）：650-661.
本文引用 [1]
69
袁志林，潘雪玉，靳微.林木共生菌系统及其作用机制：以杨树为例［J］.生态学报，2019，39（1）：381-397.
YUAN Z L， PAN X Y， JIN W.Tree-associated symbiotic microbes and underlying mechanisms of ecological interactions：a case study of poplar［J］.Acta Ecologica Sinica，2019，39（1）：381-397.
本文引用 [1]
70
QU D H， WU F L， GUO Y T，et al.Dark septate endophyte Anteaglonium sp.T010 promotes biomass accumulation in poplar by regulating sucrose metabolism and hormones［J］.Tree Physiology，2024，44（6）：tpae057.
本文引用 [1]

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