Journal of Fungi Review Physiological Basis of Smut Infectivity in the Early Stages of Sugar Cane Colonization Carlos Vicente, María-Estrella Legaz * and Elena Sánchez-Elordi Team of Intercellular Communication in Plant Symbiosis, Faculty of Biology, Complutense University, 12 José Antonio Novais Av., 28040 Madrid, Spain; [email protected] (C.V.); [email protected] (E.S.-E.) * Correspondence: [email protected]; Tel.: +34-1-3944565 Abstract: Sugar cane smut (Sporisorium scitamineum) interactions have been traditionally considered from the plant’s point of view: How can resistant sugar cane plants defend themselves against smut disease? Resistant plants induce several defensive mechanisms that oppose fungal attacks. Herein, an overall view of Sporisorium scitamineum’s mechanisms of infection and the defense mechanisms of plants are presented. Quorum sensing effects and a continuous reorganization of cytoskeletal components, where actin, myosin, and microtubules are required to work together, seem to be some of the keys to a successful attack. Keywords: actin; cytoskeleton; infectivity; myosin; quorum sensing; smut; tubulin 1. Introduction Sugarcane plants are affected by multiple microorganisms, where among them is Sporisorium scitamineum (Syd.) M. Piepenbr., M. Stoll, and F. Oberw. (Ustilago scitaminea Sydow), the causal agent of smut. It currently occurs in over 64 countries and sugarcane regions, in many of which, it causes a significant amount of damage [1]. This damage Citation: Vicente, C.; Legaz, M.-E.; increases in the sick sprouts due to secondary infections, and an increase in the size of the Sánchez-Elordi, E. Physiological Basis inoculum occurs when the whips break (a mixture of plant and fungal tissues, which is of Smut Infectivity in the Early Stages a typical structure of diseased plants) that contains spores that are spread by wind and of Sugar Cane Colonization. J. Fungi water [2], enhancing the dispersal of the pathogen. 2021, 7, 44. https://doi.org/10.3390 The plant induces several defensive mechanisms that determine the nature of the /jof7010044 interaction with the pathogen [3]. Similarly, pathogens develop mechanisms that enable them to evade and/or suppress the defensive responses of the plant [4,5]. The entry of Received: 9 December 2020 the infective mycelium into the vegetative bud meristem occurs within 6 to 36 h after Accepted: 9 January 2021 the teliospores have been deposited onto the bud scales [6]. Active penetration of fungal Published: 12 January 2021 hyphae from open stomata, floral organs, and even through the cuticle of the adaxial leaf epidermis have also been observed [7]. The cuticle can be mechanically destroyed as Publisher’s Note: MDPI stays neu- hyphae progress to the mesophilic layer of plants that are susceptible to infection [8]. tral with regard to jurisdictional clai- The subsequent growth of hyphae within the infected plant occurs mainly in the ms in published maps and institutio- parenchymatous cells of the lower internodes, achieving progress in its invasion by break- nal affiliations. ing the cell walls (Figure1). However, the pathogen can also remain in a dormant phase in the apoplastic area of the parenchymatous tissue [9]. Again, hyphae development concludes with the formation of the whip (teliospore sori) in the upper internodes. Copyright: © 2021 by the authors. Li- It has been seen that different varieties of sugar cane manifest different responses censee MDPI, Basel, Switzerland. to an attack. For example, the Barbados (B) 42,231 cultivar (cv.) is highly susceptible to This article is an open access article infection. However, Mayarí (My) 55-14 is a resistant cv. that is able to defend itself against distributed under the terms and con- attack. Numerous studies have been directed toward explaining why sugar cane varieties ditions of the Creative Commons At- respond differently to smut colonization. However, what are the triggering mechanisms tribution (CC BY) license (https:// of infection? Herein, we present the way in which the fungus tries to infect plants in the creativecommons.org/licenses/by/ early stages. 4.0/). J. Fungi 2021, 7, 44. https://doi.org/10.3390/jof7010044 https://www.mdpi.com/journal/jof J. FungiJ. Fungi 20212021, 7, ,7 x, 44FOR PEER REVIEW 2 of 18 2 of 19 A 1 mm B 300 µm FigureFigure 1. 1.( A(A) SEM) SEM micrograph micrograph of aof cross-section a cross-section of a healthyof a healthy sugar sugar cane leaf cane of leaf cv. Louisiana of cv. Louisiana 55-5. 55-5. ((BB)) SEM SEM micrograph micrograph of a of cross-section a cross-section of a smut-diseased of a smut-diseased leaf of sugar leaf caneof sugar cv. Louisiana cane cv. 55-5. Louisiana In this 55-5. In cut,this it cut, is possible it is possible to observe to observe some obturated some obturated xylem vessels xylem (red vessels arrow) (red and arrow) the subepidermal and the subepidermal and parenchymaland parenchymal tissue thattissue was that invaded was invaded by the fungal by the mycelium fungal (yellowmycelium arrow). (yellow arrow). 2. What Is the Life Cycle of the Ustilaginales-Like Sporisorium scitamineum? 2. What Is the Life Cycle of the Ustilaginales-Like Sporisorium scitamineum? First, to understand how the pathogen attacks, it is necessary to consider how its life cycleFirst, works. to understandS. scitamineum how(Syd), the pathogen previously attacks, known asit isUstilago necessary scitaminea to consider, is a basid- how its life iomycetecycle works. belonging S. scitamineum to the order (Syd), Ustilaginales, previously class known Ustilaginomycetes. as Ustilago scitaminea The life cycle, is ofa basidio- themycete smut belonging is simpler than to the that order of the Ustilaginales, rust since it is developedclass Ustilaginomycetes. on the same plant. The In life nature, cycle of the thesmut dikaryotic is simpler mycelium than that of these of the fungi rust seems since toit beis developed the cause of on its the infection same [ 10plant.,11]. Thus,In nature, the thedikaryotic primary mycelium mycelium isof saprophytic these fungi and seems of short to be duration, the cause with of its it notinfection being infectious [10,11]. Thus, the until it becomes dikaryotic through a process known as somatogamy. primary mycelium is saprophytic and of short duration, with it not being infectious until Although there are variations in the Ustilaginales’ cycles, there are some common characteristicsit becomes dikaryotic for the whole through group a (Figure process2A). known The cycle as somatogamy. includes, first, the production of teliosporesAlthough within there the host are tissue variations [12]. After in maturing,the Ustilaginales’ the teliospores, cycles, which there are are gathered some in common thecharacteristics sori, undergo for karyogamy, the whole by whichgroup their (Figure two haploid2A). The nuclei cycle fuse includes, to form afirst, diploid the [ 13production], whileof teliospores acquiring awithin thick, darkthe host wall tissue that forms [12]. a blackishAfter maturing, powdery massthe teliospores, reminiscent which of smut. are gath- eredWhen in the the sori, conditions undergo are karyogamy, adequate, the by germination which their of two the teliosporeshaploid nuclei leads fuse to the to form a formationdiploid [13], of the while pro-mycelium acquiring thata thick, the nucleusdark wall moves that toward.forms a Thisblackish will thenpowdery undergo mass remi- meiosis,niscent originatingof smut. four haploid cells (sporidia or basidiospores), which can divide asex- ually via germination, originating a variable number of sporidia. The four sporidia that are initially released, as well as the cells formed from their mitotic division, are in no case pathogenic [12]. J. Fungi 2021, 7, 44 3 of 18 J. Fungi 2021, 7, x FOR PEER REVIEW 3 of 19 B I 345 A 8 9 2 10 6 II 11 1 7 12 13 III FigureFigure 2.2. ((AA)) Life Life cycle cycle of of UstilagoUstilago maydis maydis withwith the the stages stages represented represented as asfollows: follows: (1) teliospores (1) teliospores overwintering on soil, (2) germinating teliospore, (3) basidium, (4) basidiospores, (5) infection by overwintering on soil, (2) germinating teliospore, (3) basidium, (4) basidiospores, (5) infection by the basidiospores of young plants or growing tissues in older plants, (6) leaf infection by compati- the basidiospores of young plants or growing tissues in older plants, (6) leaf infection by compatible ble basidiospores, (7) galls on leaves, (8) corn ears infection by compatible basidiospores, (9) dikar- basidiospores,yotic mycelium (7) formation, galls on leaves, (10) mycelium (8) corn earsenlarges infection and byforms compatible galls in corn basidiospores, kernels, (11) (9) mycelium dikaryotic myceliumin galls, (12) formation, dikaryotic (10) cells mycelium of mycelium enlarges become and teliospores forms galls in galls, in corn and kernels, (13) galls (11) full mycelium of telio- in galls,spores. (12) (B dikaryotic) Differences cells in ofthe mycelium life cycle of become Sporisorium teliospores sp. as in represented galls, and (13)by (I) galls sugar full cane of teliospores. meriste- (maticB) Differences infection by in thebasidiospores, life cycle of (II)Sporisorium emergencesp. of the as representedwhip-like structur by (I)e sugar from canethe shoot meristematic apical infectionmeristem, by and basidiospores, (III) billions (II)of teliospores emergence produced of the whip-like in a single structure whip. from the shoot apical meristem, and (III) billions of teliospores produced