Eur J Plant Pathol (2019) 154:157–169 https://doi.org/10.1007/s10658-018-01656-0 Plant trichomes as microbial habitats and infection sites Ki Woo Kim Accepted: 5 December 2018 /Published online: 2 January 2019 # Koninklijke Nederlandse Planteziektenkundige Vereniging 2019 Abstract Trichomes, also simply referred to as hairs, These observations indicate that plant trichomes are are fine outgrowths of epidermal cells in many organ- involved in multiple interactions in terms of providing isms including plants and bacteria. Plant trichomes have microbial habitats and infection sites as well as function- long been known for their multiple beneficial roles, ing as protective structures. Trichome-related microbial ranging from protection against insect herbivores and parasitism and endophytism can, in many ways, be con- ultraviolet light to the reduction of transpiration. How- sidered comparable to those associated with root hairs. ever, there is increasing evidence that the presence of trichomes may have detrimental consequences for Keywords Epidermis . Infection . Niche . Trichome plants. For example, plant pathogenic bacteria can enter hosts through the open bases or broken stalks of dam- aged trichomes. Similarly, trichomes are considered a Introduction preferred site for fungal infection, and in this regard, the colonization and penetration of trichomes by fungi Microbes are ubiquitous on Earth and can survive in and oomycetes have been visualized using light, fluores- even the most extreme of environments. Their habitats cence, and scanning electron microscopy in a variety of range from hydrothermal vents in the deep ocean to plants from grasses to shrubs and trees. In addition to rocks, deserts, and the poles. In addition, they consti- parasitic interactions, trichomes also form a host site for tute the microbiota within multicellular organisms. endophytic relationships with fungi, thereby serving as Identifying novel microbial habitats or ecological an unusual fungal niche. The replication and presence of niches reveals the tolerance and adaptation of microbes plant viruses in trichomes have also been confirmed after to different environments. Apart from saprophytic mi- inoculation. In contrast, the well-known beneficial crobes, pathogenic microbes continue to find ways to Azolla–Anabaena symbiosis is facilitated through epi- exploit novel host resources, be it those of humans, dermal trichomes of the seedless vascular plant Azolla. domestic animals, or plants (Engering et al. 2013). Plant pathogenic microbes enter host plants through natural openings such as stomata, lenticels, and hyda- K. W. Kim (*) thodes on plant surfaces. Moreover, some plant patho- School of Ecology and Environmental System, Kyungpook genic fungi can penetrate and infect plants directly National University, Sangju 37224, South Korea using appressoria, penetration pegs, and infection hy- e-mail: [email protected] phae. Identifying unknown infection sites and infection K. W. Kim structures can reveal novel strategies whereby patho- Tree Diagnostic Center, Kyungpook National University, gens establish compatible interactions with the host Sangju 37224, South Korea plant (Kim et al. 1999; Petkar and Ji 2017). 158 Eur J Plant Pathol (2019) 154:157–169 The surfaces of plant organs are characterized by a root hair development in Arabidopsis is known to in- variety of protuberant cellular structures including papil- volve common genes and gene products (Wagner et al. lae, trichomes, and other various emergences and pro- 2004). In this context, the microbial associations that jections (Werker 2000). These structures are distin- have been characterized for root hairs, including para- guished from others based on their ontogeny and size. sitism, endophytism, and symbiosis, might also be an- To microbes, plant surfaces studded with these structures ticipated to be features of trichomes. Trichomes have might resemble to a jungle, where epicuticular waxes been observed on all vegetative and reproductive organs form a rough terrain, veins are grooves, and trichomes in angiosperms (Ma et al. 2016); they can, for example, are trees (Vacher et al. 2016). Given that these protuber- be observed on leaf surfaces with the naked eye and are ant structures do not have natural openings in their intact responsible for the pubescence of certain leaf types state, they are not traditionally regarded as habitats or (Fig. 1). The beneficial functions ascribed to trichomes infection sites for plant pathogenic microbes. Although range from protecting the plant against insect herbivores studies have mainly focused on the beneficial roles and ultraviolet light to reducing transpiration and in- played by plant trichomes in nature, there have been an creasing tolerance to freezing (Hülskamp 2004; Kim increasing number of studies that have demonstrated 2018). Functionally, they can be classified into two trichomes to be microbial habitats and infection sites in types: (i) glandular trichomes for extracellular secretion a diversity of plants (Imboden et al. 2018; Łaźniewska of mucilage and volatile compounds, and (ii) non- et al. 2012). In this review, I aim to highlight microscopic glandular trichomes for physical defense against certain aspects of the trichome–microbe associations, both sap- stress factors. Glandular trichomes possess a basal cell, a rophytic and parasitic, involved in microbial habitation short or long stalk, and a globose secretory head (Fig. and infection in a variety of plants from grasses to shrubs 1b), whereas non-glandular trichomes are composed of and trees, thereby providing novel insights into the roles a basal cell and a long (up to 300 μm) multicellular stalk of trichomes as an often overlooked biological compo- (Kim 2013). Analytical electron microscopy has detect- nent in plant–microbe interactions. ed calcium phosphate in the non-glandular trichomes of Loasaceae plants as a structural component with antiherbivore function, comparable to the bones and Plant trichomes: structure and function teeth of animals (Ensikat et al. 2016). Plant protection chemicals are deposited on the trichomes as well as on Trichomes (from the Greek meaning Bhair^), often re- the epidermis (Fortunati and Balestra 2018). ferred to simply as hairs, are commonly described as In addition to leaves, trichomes are present on the fine outgrowths of epidermal cells in organisms. Al- surface of stems (Fig. 2a). Glandular trichomes contain though trichomes are traditionally considered to be osmiophilic compounds in the head (Fig. 2b). The stalk structures of plant origin and have been extensively of these trichomes comprises parenchymal cells beneath studied in plants, they are also innate structures of the head. Non-glandular trichomes appear as long thorns prokaryotes and eukaryotic microbes. For example, bac- on the surface, which are distinct from ribbons (Fig. 2c). terial trichomes are flexible structures comprising nu- Microtome-sectioned trichomes reveal the highly vacu- merous contiguous cells (with diameters ranging from 3 olated cells comprising the stalk (Fig. 2d). Some cells to 6 μm) containing sulfur inclusions and enveloped by may contain dense cytoplasm in light micrographs. Al- a common sheath of variable width ranging from 30 to though most trichomes have a head and a stalk filled 90 μm, as shown in mats of long filaments (Nishino with parenchymal cells, others have an empty space or et al. 1998;Danovaroetal.2017). lumen within (Tucker et al. 1984). These trichomes are Plant trichomes are unicellular or multicellular ap- referred to as cavitated or inflated trichomes, the lumen pendages that originate exclusively from epidermal cells of which can easily be mistaken for an intercellular and develop outwards on the surface of various plant space (Marinho et al. 2016). There are three types of organs (Werker 2000). This definition suggests a close domains that plant trichomes present to microbes: (i) the morphological relationship between trichomes and root trichome surface from the base to the tip, (ii) the paren- hairs, implying that aerial trichomes and Bsubterranean chymal cells within trichomes, and (iii) the trichome trichomes^ (or root hairs) cover nearly all the surfaces of lumen. Each of these domain offers different types of most plants (Wagner 1991). Moreover, trichome and nutrients and environments to the associated microbes. Eur J Plant Pathol (2019) 154:157–169 159 a living trichomes of tomato leaves have been known to be colonized by Pseudomonas syringae pv. tomato (Pietrarelli et al. 2006; Schneider and Grogan 1977). Scanning electron microcopy has also revealed the oc- currence of P. syringae pv. syringae cells at the base of trichomes (Mansvelt and Hattingh 1989), which may be related to the abundance of nutrients exuded from cracks in the cuticular layer or from the large number of ectodesmata located around the base of trichomes (Beattie and Lindow 1995). Aqueous pores ranging from 0.45 to 1.18 nm in radius are typically located in cuticular ledges at the base of trichomes (Schönherr 2006). b Entry through damaged trichomes Plant pathogenic bacteria can also gain access to plant interiors via the damaged parts of trichomes, such as opened bases or broken stalks, as infection sites. Most plant trichomes are fragile and readily collapse under slight pressure (Huang 1986), and with organ develop- ment, trichomes are gradually lost (Ma et al. 2016). P. syringae pv. syringae is known to enter pear leaves through the open base of trichomes and survive on trichomes