Biotrophic plant pathogenic fungi are widely distributed and are among the most damaging pathogenic organisms of agriculturally important crops responsible for significant losses in quality and yield. However, the pathogenesis of obligate parasitic pathogenic microorganisms is still under investigation because they cannot reproduce and complete their life cycle on an artificial medium. The successful lifestyle of biotrophic fungal pathogens depends on their ability to secrete effector proteins to manipulate or evade plant defense response. By integrating genomics, transcriptomics, and effectoromics, insights into how the adaptation of biotrophic plant fungal pathogens adapt to their host populations can be gained. Efficient tools to decipher the precise molecular mechanisms of rust–plant interactions, and standardized routines in genomics and functional pipelines have been established and will pave the way for comparative studies. Deciphering fungal pathogenesis not only allows us to better understand how fungal pathogens infect host plants but also provides valuable information for plant diseases control, including new strategies to prevent, delay, or inhibit fungal development. Our review provides a comprehensive overview of the efforts that have been made to decipher the effector proteins of biotrophic fungal pathogens and demonstrates how rapidly research in the field of obligate biotrophy has progressed.

Biotrophic plant pathogenic fungi are among the dreadful pathogens that continuously threaten the production of economically important crops. The interaction of biotrophic fungal pathogens with their hosts necessitates the development of unique infection mechanisms and involvement of various virulence-associated components. Biotrophic plant pathogenic fungi have an exceptional lifestyle that supports nutrient acquisition from cells of a living host and are fully dependent on the host for successful completion of their life cycle. The haustorium, a specialized infection structure, is the key organ for biotrophic fungal pathogens. The haustorium is not only essential in the uptake of nutrients without killing the host, but also in the secretion and delivery of effectors into the host cells to manipulate host immune system and defense responses and reprogram the metabolic flow of the host. Although there is a number of unanswered questions in this area yet, results from various studies indicate that the haustorium is the root of biotrophic fungal pathogens. This review provides an overview of current knowledge of the haustorium, its structure, composition, and functions, which includes the most recent haustorial transcriptome studies.

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Wheat is one of the most important staple foods on earth. Leaf rust, stem rust and stripe rust, caused by Puccini triticina, Puccinia f. sp. graminis and Puccinia f. sp. striiformis, respectively, continue to threaten wheat production worldwide. Utilization of resistant cultivars is the most effective and chemical-free strategy to control rust diseases. Convectional and molecular biology techniques identified more than 200 resistance genes and their associated markers from common wheat and wheat wild relatives, which can be used by breeders in resistance breeding programmes. However, there is continuous emergence of new races of rust pathogens with novel degrees of virulence, thus rendering wheat resistance genes ineffective. An integration of genomic selection, genome editing, molecular breeding and marker-assisted selection, and phenotypic evaluations is required in developing high quality wheat varieties with resistance to multiple pathogens. Although host genotype resistance and application of fungicides are the most generally utilized approaches for controlling wheat rusts, effective agronomic methods are required to reduce disease management costs and increase wheat production sustainability. This review gives a critical overview of the current knowledge of rust resistance, particularly race-specific and non-race specific resistance, the role of pathogenesis-related proteins, non-coding RNAs, and transcription factors in rust resistance, and the molecular basis of interactions between wheat and rust pathogens. It will also discuss the new advances on how integrated rust management methods can assist in developing more durable resistant cultivars in these pathosystems.

Fungal plant pathogens use proteinaceous effectors as well as newly identified secondary metabolites (SMs) and small non-coding RNA (sRNA) effectors to manipulate the host plant’s defense system via diverse plant cell compartments, distinct organelles, and many host genes. However, most molecular studies of plant–fungal interactions have focused on secreted effector proteins without exploring the possibly equivalent functions performed by fungal (SMs) and sRNAs, which are collectively known as “non-proteinaceous effectors”. Fungal SMs have been shown to be generated throughout the plant colonization process, particularly in the early biotrophic stages of infection. The fungal repertoire of non-proteinaceous effectors has been broadened by the discovery of fungal sRNAs that specifically target plant genes involved in resistance and defense responses. Many RNAs, particularly sRNAs involved in gene silencing, have been shown to transmit bidirectionally between fungal pathogens and their hosts. However, there are no clear functional approaches to study the role of these SM and sRNA effectors. Undoubtedly, fungal SM and sRNA effectors are now a treasured land to seek. Therefore, understanding the role of fungal SM and sRNA effectors may provide insights into the infection process and identification of the interacting host genes that are targeted by these effectors. This review discusses the role of fungal SMs and sRNAs during plant-fungal interactions. It will also focus on the translocation of sRNA effectors across kingdoms, the application of cross-kingdom RNA interference in managing plant diseases and the tools that can be used to predict and study these non-proteinaceous effectors.

ABC transporters play important roles in plant growth and resistance to abiotic and biotic stresses. Here, we showed that the TaABCG36 gene positively regulates leaf rust resistance in the wheat line Thatcher + Lr19 (TcLr19) when challenged with an avirulent pathotype of Puccinia triticina (Pt). The TaABCG36 gene was cloned from genomic DNA and cDNA from wheat line TcLr19. The clone was 6730 bp in gDNA and 4365 bp in cDNA for this gene. It encoded an ABC transporter with 1454 amino acids in length. BLASTp analysis indicated a considerable identity ABC transporter G family member 36 with Aegilops tauschii subsp. strangulata, Triticum dicoccoides, and T. aestivum; thus, we named the gene TaABCG36. TaABCG36 was proved to be a plasma transmembrane protein by bioinformatic analysis and subcellular localization of the TaABCG36–GFP fusion protein. The expression of TaABCG36 in wheat leaves reached a peak at 72 h post-inoculation by Pt avirulence pathotype, and the expression was also induced by phytohormone treatments of salicylic acid (SA), abscisic acid (ABA), and methyl jasmonate (MeJA). Three fragments (V1–V3) of the TaABCG36 gene were introduced to the BSMV-VIGS vector and, thus, silenced the expression of TaABCG36 in the wheat line TcLr19. All the three BSMV:VIGS-infected plants showed reaction type “3” to Pt pathotype THTS, which was fully avirulent on TcLr19 (infection type “0”). Histopathological observation showed that silencing of TaABCG36 facilitated the formation of haustorial mother cells (HMC) and mycelial growth, implying that TaABCG36 plays a positive role in the response of TcLr19 against THTS. These results provide molecular insight into the interaction between Pt and its wheat host and identify a potential target for engineering resistance in wheat to damaging pathogen of Pt.

Wheat leaf rust, caused by Puccinia triticina Eriks. (Pt), is a global wheat disease threatening wheat production. Dissecting how Pt effector proteins interact with wheat has great significance in understanding the pathogenicity mechanisms of Pt. In the study, the cDNA of Pt 13-5-72 interacting with susceptible cultivar Thatcher was used as template to amplify Pt13024 gene. The expression pattern and structure of Pt13024 were analyzed by qRT-PCR and online softwares. The secretion function of Pt13024 signal peptide was verified by the yeast system. Subcellular localization of Pt13024 was analyzed using transient expression on Nicotiana benthamiana. The verification that Pt13024 inhibited programmed cell death (PCD) was conducted on N. benthamiana and wheat. The deletion mutation of Pt13024 was used to identify the virulence function motif. The transient transformation of wheat mediated by the type III secretion system (TTSS) was used to analyze the activity of regulating the host defense response of Pt13024. Pt13024 gene silencing was performed by host-induced gene silencing (HIGS). The results showed that Pt13024 was identified as an effector and localized in the cytoplasm and nucleus on the N. benthamiana. It can inhibit PCD induced by the Bcl-2-associated X protein (BAX) from mice and infestans 1 (INF1) from Phytophthora infestans on N. benthamiana, and it can also inhibit PCD induced by DC3000 on wheat. The amino acids 22 to 41 at N-terminal of the Pt13024 are essential for the inhibition of programmed cell death (PCD) induced by BAX. The accumulation of reactive oxygen species and deposition of callose in near-isogenic line TcLr30, which is in Thatcher background with Lr30, induced by Pt13024 was higher than that in 41 wheat leaf rust-resistant near-isogenic lines (monogenic lines) with different resistance genes and Thatcher. Silencing of Pt13024 reduced the leaf rust resistance of Lr30 during the interaction between Pt and TcLr30. We can conclude that Pt13024 is avirulent to TcLr30 when Pt interacts with TcLr30. These findings lay the foundation for further investigations into the role of Pt effector proteins in pathogenesis and their regulatory mechanisms.

Wheat powdery mildew caused by a biotrophic fungus Blumeria graminis f. sp. tritici (Bgt), is a widespread airborne disease which continues to threaten global wheat production. One of the most chemical-free and cost-effective approaches for the management of wheat powdery mildew is the exploitation of resistant cultivars. Accumulating evidence has reported that more than 100 powdery mildew resistance genes or alleles mapping to 63 different loci (Pm1-Pm68) have been identified from common wheat and its wild relatives, and only a few of them have been cloned so far. However, continuous emergence of new pathogen races with novel degrees of virulence renders wheat resistance genes ineffective. An essential breeding strategy for achieving more durable resistance is the pyramiding of resistance genes into a single genotype. The genetics of host-pathogen interactions integrated with temperature conditions and the interaction between resistance genes and their corresponding pathogen a virulence genes or other resistance genes within the wheat genome determine the expression of resistance genes. Considerable progress has been made in revealing Bgt pathogenesis mechanisms, identification of resistance genes and breeding of wheat powdery mildew resistant cultivars. A detailed understanding of the molecular interactions between wheat and Bgt will facilitate the development of novel and effective approaches for controlling powdery mildew. This review gives a succinct overview of the molecular basis of interactions between wheat and Bgt, and wheat defense mechanisms against Bgt infection. It will also unleash the unsung roles of epigenetic processes, autophagy and silicon in wheat resistance to Bgt.