How Do Smut Fungi Use Plant Signals to Spatiotemporally Orientate on and In Planta?

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.

Ethylene Promotes Expression of the Appressorium- and Pathogenicity-Related Genes via GPCR- and MAPK-Dependent Manners in Colletotrichum gloeosporioides

“…Besides ET, many other host-plant-related materials may stimulate spore germination and appressoria differentiation of pathogenic fungi, such as adhesives, cutin monomers, surface hydrophobicity, surface hardness, and topographic signals [ 83 , 84 ]. Several signal pathways participate in regulating the appressorium formation, such as Gα and Gβ proteins [ 33 ], the adenylyl cyclase and PKA-mediated cAMP pathway [ 85 ], calmodulin signaling [ 86 ], and the MAPK signaling pathway [ 37 ].…”

The barley HvSTP13GR mutant triggers resistance against biotrophic fungi

“…Support for this scenario comes from the observation that diverse fungal pathogens express one or several haustorial glucose transporters that are important for fungal virulence. Furthermore, it was hypothesized that glucose is not only used as an energy source but also functions as a signal molecule for fungal growth (Chang et al, 2020 ; van der Linde & Göhre, 2021 ; Sosso et al, 2019 ; Voegele et al, 2001 ). Additionally, fungi secrete invertases, whose activity might further increase the supply of monosaccharides at the interaction surface (Chang et al, 2017 ; Voegele et al, 2006 ).…”

Infection Strategies and Pathogenicity of Biotrophic Plant Fungal Pathogens

“…Effectors of biotrophic fungi also bind directly to the host DNA promoter, thereby regulating or altering its transcriptional processes, resulting in defective defense genes ( Ahmed et al, 2018 ). Moreover, the effectors of biotrophic fungi camouflage the host as modulators, leading to the diversion of the metabolic flux of many compounds, resulting in a deficiency of precursors or compounds responsible for host defense ( Tanaka et al, 2014 ; van der Linde and Göhre, 2021 ). Some well-known other examples are: CSEP0055 ( Zhang et al, 2012 ), BEC3, BEC4 ( Schmidt et al, 2014 ), CSEP0105, CSEP0162 ( Ahmed et al, 2015 ), BEC1054 ( Pennington et al, 2016 ), BEC1019 ( Zhang et al, 2019 ), CSEP0027 ( Yuan et al, 2021 ), CSEP0139 and CSEP0182 ( Li et al, 2021 ) from Bgh and AvrPm3 a 1/ f 1 from Bgt ( Bourras et al, 2015 ; Parlange et al, 2015 ).…”