Research Article: Comparative transcriptome profiling of Blumeria graminis f. sp. tritici during compatible and incompatible interactions with sister wheat lines carrying and lacking Pm40

Date Published: July 5, 2018

Publisher: Public Library of Science

Author(s): Yuting Hu, Yinping Liang, Min Zhang, Feiquan Tan, Shengfu Zhong, Xin Li, Guoshu Gong, Xiaoli Chang, Jing Shang, Shengwen Tang, Tao Li, Peigao Luo, Dragan Perovic.


Blumeria graminis f. sp. tritici (Bgt) is an obligate biotrophic fungus that causes wheat powdery mildew, which is a devastating disease in wheat. However, little is known about the pathogenesis of this fungus, and differences in the pathogenesis of the same pathogen at various resistance levels in hosts have not been determined. In the present study, leaf tissues of both Pm40-expressing hexaploid wheat line L658 and its Pm40-deficient sister line L958 were harvested at 0 (without inoculation), 6, 12, 24, 48 and 72 hours post-inoculation (hpi) with Bgt race 15 and then subjected to RNA sequencing (RNA-seq). In addition, we also observed changes in fungal growth morphology at the aforementioned time points. There was a high correlation between percentage of reads mapped to the Bgt reference genome and biomass of the fungus within the leaf tissue during the growth process. The percentage of mapped reads of Bgt in compatible interactions was significantly higher (at the p<0.05 level) than that of reads in incompatible interactions from 24 to 72 hpi. Further functional annotations indicated that expression levels of genes encoding H+-transporting ATPase, putative secreted effector proteins (PSEPs) and heat shock proteins (HSPs) were significantly up-regulated in compatible interactions compared with these levels in incompatible interactions, particularly at 72 hpi. Moreover, Kyoto Encyclopedia of Genes and Genomes (KEGG) pathway analysis suggested that genes involved in the endocytosis pathway were also enriched in compatible interactions. Overall, genes encoding H+-transporting ATPase, PSEPs and HSPs possibly played crucial roles in successfully establishing the pathogenesis of compatible interactions during late stages of inoculation. The study results also indicated that endocytosis is likely to play a potential role in Bgt in establishing compatible interactions.

Partial Text

Powdery mildew fungi (Ascomycetes, Erysiphales) infect more than 10,000 plant species [1], one of which is Blumeria graminis f. sp. tritici (Bgt), an obligate biotrophic fungus that grows and reproduces only on living wheat (Triticum aestivum L.), which is an economically important agricultural crop that is in high demand around the world [2]. Powdery mildew caused by Bgt has seriously reduced wheat production both in China and around the world [3–5]. To control wheat powdery mildew, 80 powdery mildew resistance (Pm) alleles have been identified at 53 gene loci in wheat and its relatives, most of which confer race-specific resistance [6,7]. In contrast, only one avirulence gene in Bgt, named AvrPm3a/f, is recognized by the Pm3a and Pm3f alleles and has been cloned [8], and an allele-unspecific pathogen-encoded suppressor of avirulence named SvrPm3a1/f1 also has been cloned [9]. Both AvrPm3a/f and SvrPm3a1/f1 have similar expression kinetics, with a peak at haustorium formation, and only the inactive suppressor and sufficient amounts of AVR protein can active the R gene [8,10]. Similarly, in Blumeria graminis f. sp. hordei (Bgh), which is the other forma specialis of Blumeria graminis, only two avirulence genes, Avra10 and Avrk1, have been cloned. Both genes are derived from non-LTR retrotransposons [11,12], and their limited homology at the DNA and protein level indicates that they arose from distantly related LINE families [13]. Comparatively, the pathogenesis of Bgt is more unclear than the resistance mechanism of wheat.

Although several studies have investigated powdery mildew pathogens in both barley and Arabidopsis [33,34,24,20], fewer studies have investigated the Bgt pathogen in wheat [15, 38]. In present study, the different transcript expression patterns of Bgt during compatible and incompatible interactions and the relationships with fungal morphological growth have been determined.

The percentage of reads mapped to the Bgt reference genome was very low for all time points of compatible and incompatible interactions, but there were high correlations with fungal biomass. These results potentially suggest that the differences in morphological growth were accompanied by differences in gene expression at the transcriptome level. At early infection stages, H+-transporting ATPase may act as the key for entering hosts, which involves first breaking through the host defenses in compatible interactions while functioning similarly to incompatible interactions without the key to enter the host. After Bgt entered the host, it formed haustoria. The high expression of PSEPs and HSPs may indicate that most possibly acted as virulence factors to enhance pathogenicity at this stage. However, the insufficient accumulation of PSEPs and HSPs in incompatible interactions resulted in a weak attack on the host. At later infection stages, PSEPs and HSPs were possibly used to suppress the host defense response. In addition, H+-transporting ATPase may be involved in nutrient uptake at later infection stages in compatible interaction. Overall, H+-transporting ATPase, PSEPs and HSPs may play a vital role in successfully establishing pathogenesis among compatible interactions. Furthermore, endocytosis is likely an important pathway for exchanging substances as the pathogen interacts with the host.




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