How Do Smut Fungi Use Plant Signals to Spatiotemporally Orientate on and in Planta?
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Journal of Fungi Review How Do Smut Fungi Use Plant Signals to Spatiotemporally Orientate on and In Planta? Karina van der Linde 1,*,† and Vera Göhre 2,*,† 1 Department of Cell Biology and Plant Biochemistry, University of Regensburg, 93053 Regensburg, Germany 2 Institute for Microbiology, Cluster of Excellence on Plant Sciences, Heinrich-Heine University, 40225 Düsseldorf, Germany * Correspondence: [email protected] (K.v.d.L.); [email protected] (V.G.) † These authors contributed equally to this work. Abstract: Smut fungi represent a large group of biotrophic plant pathogens that cause extensive yield loss and are also model organisms for studying plant–pathogen interactions. In recent years, they have become biotechnological tools. After initial penetration of the plant epidermis, smut fungi grow intra—and intercellularly without disrupting the plant-plasma membrane. Following the colonialization step, teliospores are formed and later released. While some smuts only invade the tissues around the initial penetration site, others colonize in multiple plant organs resulting in spore formation distal from the original infection site. The intimate contact zone between fungal hyphae and the host is termed the biotrophic interaction zone and enables exchange of signals and nutrient uptake. Obviously, all steps of on and in planta growth require fine sensing of host conditions as well as reprogramming of the host by the smut fungus. In this review, we highlight selected examples of smut fungal colonization styles, directional growth in planta, induction of spore formation, and the signals required, pointing to excellent reviews for details, to draw attention to some of the open questions in this important research field. Citation: van der Linde, K.; Göhre, V. How Do Smut Fungi Use Plant Keywords: Ustilago; Microbotryum; Sporisorium; Thecaphora; nutrition; meristem; growth; develop- Signals to Spatiotemporally Orientate ment on and In Planta?. J. Fungi 2021, 7, 107. https://doi.org/10.3390/ jof7020107 1. Introduction Academic Editors: Michael H. Perlin, More than 1000 teliospore-forming fungi, which cause plant smut diseases, have Barry J. Saville and Jan Schirawski been identified so far. The term smut stems from the German term “schmutzig” (English: Received: 23 December 2020 dirty) and regards the appearance of infected plant material, which is caused by a massive Accepted: 23 January 2021 amount of black, melanized teliospores. The vast majority of smut fungi infect angiosperms, Published: 2 February 2021 and while most prefer annuals, some infect perennial plants [1]. Commonly, smuts are biotrophic pathogens exhibiting a narrow host range. Besides conventional phylogenetic Publisher’s Note: MDPI stays neutral classification, the smuts can be separated into three groups: (1) smut fungi that infect with regard to jurisdictional claims in locally and form teliospores at the original penetration site; (2) smut fungi that infect published maps and institutional affil- systemically and colonize several tissues of their host, with teliospore production distant iations. from the infection site; (3) smut fungi that can infect both locally and systemically (Figure1) . Furthermore, the life cycle of the host plant, e.g., annual vs. perennial, and the infected plant tissues, e.g., aerial vs. below-ground, are valuable points of comparison, since they differ in plant signals providing cues for the fungus (Figure1). In this review, we compare Copyright: © 2021 by the authors. the different infection strategies used by smut fungi and summarize the underlying signals Licensee MDPI, Basel, Switzerland. that enable spatiotemporal orientation of the fungus on and in the plant. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https:// creativecommons.org/licenses/by/ 4.0/). J. Fungi 2021, 7, 107. https://doi.org/10.3390/jof7020107 https://www.mdpi.com/journal/jof J. Fungi 2021, 7, 107 2 of 13 J. Fungi 2021, 7, x FOR PEER REVIEW 2 of 13 Figure 1. Overview of the different smuts discussed in this review. For each smut, the initial pene- Figure 1. Overview of the different smuts discussed in this review. For each smut, the initial tration sites and the site of teliospore formation is indicated. T. thlaspeos and S. scitamineum over- penetration sites and the site of teliospore formation is indicated. T. thlaspeos and S. scitamineum winter inside the host. U. esculenta is transmitted via the rhizome. overwinter inside the host. U. esculenta is transmitted via the rhizome. 2.2. Smut Smut Fungi Fungi Differ Differ in in Their Their Infection Infection Strategies Strategies ToTo colonize colonize their their host host plant, plant, all all smut smut fungi fungi face face the the initial initial challenge challenge of of penetrating penetrating thethe plant plant tissue, tissue, and and subsequently subsequently need need to to proliferate proliferate to to ultimately ultimately sporulate sporulate for for fungal fungal propagationpropagation (Figure (Figure1). 1). The The life life cycle cycle is is best best characterized characterized in in the the model model smut smut fungus fungusU. U. maydismaydis[2 ].[2]. Teliospores Teliospores landing landing on a planton a surfaceplant surface germinate, germinate, giving rise giving to haploid rise to sporidia haploid thatsporidia can proliferate that can proliferate asexually. asex Pathogenicually. Pathogenic development development of U. maydis of U.starts maydis with starts mating with ofmating sporidia, of sporidia, which leads which to theleads formation to the formation of an infectious, of an infectious, dikaryotic dikaryotic filament filament [3]. This [3]. filamentThis filament is arrested is arrested in the in G2 the phase G2 phase of the of cell the cycle cell cycle [4], and [4], strongand strong polar polar tip growth tip growth is supportedis supported by insertion by insertion of retraction of retraction septa septa at the at basalthe basal pole pole while while maintaining maintaining cytoplasmic cytoplas- continuitymic continuity [5]. Both [5]. theBoth cell the cycle cell cycle arrest arrest and septationand septation are required are required for the for formationthe formation of appressoriaof appressoria for penetrationfor penetration [6]. [6]. These These appressoria appressoria are are non-melanized non-melanized and and do do not not build build upup turgor turgor pressure, pressure, butbut ratherrather relyrely on plan plant-cell-wall-degradingt-cell-wall-degrading enzymes enzymes [7] [7 ]that that are are in- inducedduced by by plant surface cues suchsuch asas thethe hydrophobichydrophobic surfacesurface and and cutin cutin monomers monomers [ 8[8].]. SuccessfulSuccessful penetration penetration of of the the cuticle cuticle leads leads to to re-activation re-activation of of the the cell cell cycle cycle without without nuclear nuclear fusionfusion and and subsequent subsequent local local biotrophicbiotrophic proliferation of of the the dikaryotic dikaryotic filament. filament. During During the thebiotrophic biotrophic phase, phase, hyphae hyphae grow grow inter—and inter—and intracellularly intracellularly in in the the plant plant tissues. tissues. Several Several re- reviewsviews describe describe effector effector translocation translocation and and its its ac activitytivity in in suppressing suppressing the the host-defense host-defense re- responsessponses during during the the biotrophic biotrophic phase phase [9–11]. [9–11 In].duction Induction of plant of plant tumors tumors depends depends on specific on specificeffectors, effectors, such as such See1 as (seedling See1 (seedling efficient efficient effector effector 1) [12] 1), but [12 ],isbut independent is independent of the of subse- the subsequentquent sporulation sporulation that thatis controlled is controlled by the by tr theanscription transcription factor factor ROS1 ROS1 (regulator (regulator of sporo- of sporogenesisgenesis 1) [13]. 1) [ 13Ultimately,]. Ultimately, karyogamy karyogamy and and sporulation sporulation occur occur in inthe the tissue tissue adjacent adjacent to tothe thepenetration penetration site site as asearly early as as within within 12 12 days days [14]. [14 ].This This makes makes U.U. maydis maydis aa representative representative of ofthe the locally locally infecting infecting smut smut fungi. fungi. Organ-specific,Organ-specific, local local infection infection also also occurs occurs when whenMicrobotryum Microbotryumspecies species infect infect flowers flowers of theof whitethe white campion, campion,Silene Silene latifolia latifolia(Figure (Figure1). Upon1). Upon invasion invasion of maleof male flowers, flowers, the the fungus fungus sporulatessporulates in in pollen pollen sacs. sacs. During During the the infection infection of of female female flowers, flowers, these these are are turned turned into into a a malemale morphology morphology to to promote promote fungal fungal proliferation proliferation [15 [15,16].,16]. In In addition, addition,Microbotryum Microbotryumis is also able to grow systemically when it infects seedlings [17]. Interestingly, the germination J. Fungi 2021, 7, 107 3 of 13 also able to grow systemically when it infects seedlings [17]. Interestingly, the germination pattern of teliospores differs between seedlings and flowers. Germination of seedlings leads to immediate mating and penetration of the host plant in the filamentous form, while germination in flowers