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The stem rust fungus Puccinia graminis f. sp. tritici induces waves of small RNAs with opposing profiles during wheat infection
Background: The fungus Puccinia graminis f. sp. tritici (Pgt) causes devastating stem rust disease on wheat. Infection occurs when rust spores germinate on the leaf surface and subsequently, specialized infection structures called haustoria form inside host cells. Small RNAs (sRNAs) are critical regulators of gene expression and can play a significant role in plant-pathogen crosstalk. How Pgt utilizes sRNAs during infection is thus far unknown. Results: Small RNA and transcriptome sequencing during Pgt-wheat infection reveals that the Pgt RNA interference (RNAi) machinery has functionally diversified. A number of Pgt RNAi genes are strongly up-regulated during late infection and in haustorial tissue and this coincides with the production of distinct Pgt sRNA profiles during infection. Strikingly, over 90% of Pgt sRNAs are differentially expressed during infection, compared to only 2% of wheat sRNAs. An early wave of Pgt sRNAs expressed during infection constitutes of 21 nt sRNAs with a 5' uracil derived from genes, whereas the late wave of Pgt sRNAs encompasses 22 nt sRNAs with a 5' adenine derived from repetitive regions. The late wave of Pgt sRNAs appears to target largely transposable elements and genes located in close proximity to TEs targeted by sRNAs exhibit reduced average expression, resembling the epigenetic silencing mechanism in plants. Conclusion: We conclude that the Pgt RNAi machinery has functionally diversified and is highly regulated, resulting in differential accumulation of Pgt sRNAs in germinated spores and specialized-infection tissues. Such tight temporal control of the RNAi machinery has thus far not been observed in fungi.
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