Fungal Pathogen Emergence: Investigations with an Ustilago maydis × Sporisorium reilianum Hybrid

Abstract

The emergence of new fungal pathogens threatens sustainable crop production worldwide. One mechanism by which new pathogens may arise is hybridization. To investigate hybridization, the related smut fungi, Ustilago maydis and Sporisorium reilianum, were selected because they both infect Zea mays, can hybridize, and tools are available for their analysis. The hybrid dikaryons of these fungi grew as filaments on plates but their colonization and virulence in Z. mays were reduced compared to the parental dikaryons. The anthocyanin induction caused by the hybrid dikaryon infections was distinct, suggesting its interaction with the host was different from that of the parental dikaryons. Selected virulence genes previously characterized in U. maydis and their predicted S. reilianum orthologs had altered transcript levels during hybrid infection of Z. mays. The downregulated U. maydis effectors, tin2, pit2, and cce1, and transcription factors, rbf1, hdp2, and nlt1, were constitutively expressed in the hybrid. Little impact was observed with increased effector expression; however, increased expression of rbf1 and hdp2, which regulate early pathogenic development by U. maydis, increased the hybrid’s capacity to induce symptoms including the rare induction of small leaf tumors. These results establish a base for investigating molecular aspects of smut fungal hybrid pathogen emergence.

Construction and analysis of gene co-expression network in the pathogenic fungus Ustilago maydis

“…On the other hand, in the Darkmagenta module the MCM10-essential chromatin-associated protein involved in the initiation of DNA replication (UMAG_10135), and Putative DNA polymerase epsilon (UMAG_01008) with a degree of 39, were identified as hubs. These genes are related to the replication process, which agrees with functions found in the enriched analysis ( Araki et al, 1992 ; Storfie and Saville, 2021 ). Moreover, another interesting hub is UMAG_05113 in the Grey60 module, it codes for Threonine dehydratase which is a key enzyme in BCAA synthesis, which catalyzes the conversion L-threonine into α-ketobutyrate, furthermore, this enzyme is inhibited by the end product of the metabolic pathway ( Liang et al, 2021 ).…”

The Novel Effector Ue943 Is Essential for Host Plant Colonization by Ustilago esculenta

“…For example, in Ustilago maydis, Tin2 can be utilized to stimulate the production of anthocyanins and reduce salicylic acid in local plant tissues, thus facilitating long-term colonization of the host plant [1]; Pit2 inhibits a group of apoplastic maize cysteine proteases, thereby suppressing plant defense responses [2]; Pep1 inhibits the activity of plant peroxidase enzymes involved in the production of reactive oxygen species (ROS) [3]; and See1 is necessary for U. maydis-induced reactivation of plant DNA synthesis during leaf tumor progression [4]. It is worth noting that Tin2 secreted by U. maydis and Sporisorium reilianum suppresses plant defense in different ways [5]. It indicates that some effectors can acquire a specialized function during coevolution with host plants [6].…”