Forest Tree Microbiomes and Associated Fungal Endophytes: Functional Roles and Impact on Forest Health
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Review Forest Tree Microbiomes and Associated Fungal Endophytes: Functional Roles and Impact on Forest Health Eeva Terhonen 1, Kathrin Blumenstein 1 , Andriy Kovalchuk 2 and Fred O. Asiegbu 2,* 1 Forest Pathology Research Group, Büsgen-Institute, Department of Forest Botany and Tree Physiology, Faculty of Forest Sciences and Forest Ecology, University of Göttingen, Büsgenweg 2, 37077 Göttingen, Germany; [email protected] (E.T.); [email protected] (K.B.) 2 Department of Forest Sciences, P.O. box 27, University of Helsinki, FIN-00014 Helsinki, Finland; andriy.kovalchuk@helsinki.fi * Correspondence: fred.asiegbu@helsinki.fi; Tel.: +358-2941-58109 Received: 27 November 2018; Accepted: 1 January 2019; Published: 9 January 2019 Abstract: Terrestrial plants including forest trees are generally known to live in close association with microbial organisms. The inherent features of this close association can be commensalism, parasitism or mutualism. The term “microbiota” has been used to describe this ecological community of plant-associated pathogenic, mutualistic, endophytic and commensal microorganisms. Many of these microbiota inhabiting forest trees could have a potential impact on the health of, and disease progression in, forest biomes. Comparatively, studies on forest tree microbiomes and their roles in mutualism and disease lag far behind parallel work on crop and human microbiome projects. Very recently, our understanding of plant and tree microbiomes has been enriched due to novel technological advances using metabarcoding, metagenomics, metatranscriptomics and metaproteomics approaches. In addition, the availability of massive DNA databases (e.g., NCBI (USA), EMBL (Europe), DDBJ (Japan), UNITE (Estonia)) as well as powerful computational and bioinformatics tools has helped to facilitate data mining by researchers across diverse disciplines. Available data demonstrate that plant phyllosphere bacterial communities are dominated by members of only a few phyla (Proteobacteria, Actinobacteria, Bacteroidetes). In bulk forest soil, the dominant fungal group is Basidiomycota, whereas Ascomycota is the most prevalent group within plant tissues. The current challenge, however, is how to harness and link the acquired knowledge on microbiomes for translational forest management. Among tree-associated microorganisms, endophytic fungal biota are attracting a lot of attention for their beneficial health- and growth-promoting effects, and were preferentially discussed in this review. Keywords: microbiota; microbiome; endophytes; fungi; forest trees 1. What are Microbiomes Land plants are ubiquitously associated with various microorganisms. The communities of fungi, bacteria, archaea, and protists colonizing plant tissues and inhabiting outer plant surfaces, collectively comprise plant microbiota [1]. Different plant tissues host distinct plant communities, which are commonly divided into the rhizosphere (microbial communities associated with root surface and adjacent soil layer), phyllosphere (microbial communities of outer surfaces of aerial plant parts) and endosphere (microbial communities residing within plant tissues) [1]. The plant microbiome (phytobiome), in turn, is defined as a full set of microbial genomes associated with a host plant [2]. The importance of plant-associated microbes for host plant fitness, health and nutrition is universally accepted [3]. In particular, certain fungi and bacteria promote plant growth and increase Forests 2019, 10, 42; doi:10.3390/f10010042 www.mdpi.com/journal/forests Forests 2019, 10, 42 2 of 33 Forests 2018, 9, x FOR PEER REVIEW 2 of 32 theirtheir stress stress resistance resistance [4]. However, [4]. However, not all symbiotic not all symbiotic organisms organismsprovide ben provideefits to the benefits host, as to plant the- host, microbialas plant-microbial interactions interactionscan also be can neutral also be (commonly neutral (commonly referred referred to as commensalism) to as commensalism) or even or even deleteriousdeleterious for the for hos thet host (parasitism (parasitism or pathogenicity) or pathogenicity) [4,5]. [4 The,5]. Theoverall overall impact impact of plant of plant-associated-associated microbesmicrobes on host on hosthealth health and andfitness fitness is determined is determined by a bynumber a number of factors, of factors, which which include include host hostand and microbialmicrobial genotypes, genotypes, interactions interactions within within microbiota microbiota and andvarious various abiotic abiotic factor factorss [4]. [4]. The Thecollecti collectiveve efforts efforts of research of research groups groups working working in the in field the resulted field resulted in the in accumulation the accumulation of a of considerablea considerable amount amount of knowledge of knowledge about the about diversity the diversity of microorganisms of microorganisms (mainly bacteria (mainly and bacteria fungi) and associatedfungi) associatedwith the model with theplants model and plants the important and the important agricultural agricultural crops. At crops. the same At thetime, same our time, knowledgeour knowledge of microbiota of microbiota associated associated with other with plant other species plant species is still islimited still limited and often and oftenfragmentary, fragmentary, eveneven in the in thecase case of the of themost most common common species species of oftemperate temperate and and boreal boreal forests forests [6]. [6]. When When comparing comparing the the numbersnumbers of publications associated with “microbiome”,“microbiome”, “microbiota”“microbiota” oror “metagenomics”,“metagenomics”, andand also also combiningcombining oneone of these terms with either either “human”, “human”, “agricultural “agricultural crops” crops” or or “ “agriculturalagricultural crops crops or or plants”plants” or or “forest “forest trees” trees” between between the the decades decades of 1998 of 1998–2008–2008 and and 2009 2009–2018,–2018, the theimmense immense increase increase indicatesindicates the increasing the increasing level level of interest of interest (Figure (Figure 1). 1). 100000 10000 1000 100 10 1 Microbiome Microbiome Number of hits in Web Scienceof Web in hitsofNumber Microbiome Microbiome or Microbiota or Microbiota or Microbiota or Microbiota or or or Microbiome Microbiota Metagenomics or Metagenomics Metagenomics Metagenomics Metagenomics and and and Forest and Human Agricultural Agricultural trees crops crops or Plants 2009-2018 18465 38346 5220 16069 189 3726 116 1998-2008 106 3398 296 1035 11 271 12 FigureFigure 1. Total 1. Total number number of microbiome of microbiome,, microbiota microbiota or metagenomics or metagenomics associated associated peer- peer-reviewedreviewed articles articles for human,for human, agricultural agricultural crops, crops, plants plants or forest or forest trees trees from from 1998 1998–2008–2008 and and2009 2009–2018.–2018. 2. Insights2. Insights from from Agricultural Agricultural Crops Crops and andHuman Human Microbiome Microbiome Projects Projects It hasIt hasbeen been acknowledged acknowledged that thathuman human microbio microbiotata play playkey keyroles roles in human in human health health and anddisease disease progressionprogression [7]. [The7]. Theincreasing increasing interest interest in the in exploration the exploration of human of human microbiome microbiome has hasboosted boosted the the developmentdevelopment of corresponding of corresponding techniques, techniques, methodological methodological approaches, approaches, experimental experimental procedures and and computationalcomputational toolstools applicable applicable to to forest forest biomes. biomes In. In turn, turn, the the studies studies of of plant plant microbiomes microbiomes could could greatly greatlybenefit benefit from from the the progress progress achieved achieved in in the the understanding understanding of of the thehuman human microbiomemicrobiome and from the the technicaltechnical advances inin thethe field.field. Currently,Currently, the the focus focus in in studies studies of of plant plant microbial microbial communities communities is shifted is shiftedfrom from the initialthe initial descriptive descriptive phase towardsphase towards mechanisms mechanisms controlling controlling the assembly the andassembly functioning and of functioningmicrobiota, of microbiota, the functional the rolefunctional of individual role of componentsindividual components and the possible and the applications possible applications in the integrated in theplant integrated management plant management plans. plans. MetagenomeMetagenome-wide-wide association association studies studies (MWAS) (MWAS) constitute constitute one oneof the of theimportant important approaches approaches towardstowards better better understanding understanding of the of functional the functional role of role individual of individual components components of microbiome of microbiomes.s. In MWAS, a possible association between a relative abundance of a given gene in the metagenome and an occurrence of a disease of interest is analyzed [8]. MWAS is widely used to study associations Forests 2019, 10, 42 3 of 33 In MWAS, a possible association between a relative abundance of a given gene in the metagenome and an occurrence of a disease of interest is analyzed [8]. MWAS is widely used to study associations between microbiome and human diseases, such as type-2 diabetes, rheumatoid arthritis, and obesity [8]. The successForests 2018 achieved,