Abstract
Rice false smut caused by Ustilaginoidea virens is a serious disease of rice (Oryza sativa), severely reducing plant mass and yields worldwide. We performed genome-wide analysis of the CCHC-type zinc-finger transcription factor family in this pathogen. We identified and functionally characterized seven UvCCHC genes in U. virens. The deletion of various UvCCHC genes affected the stress responses, vegetative growth, conidiation, and virulence of U. virens. ∆UvCCHC5 mutants infected rice spikelets normally but could not form smut balls. Sugar utilization experiments showed that the ∆UvCCHC5 mutants were defective in the utilization of glucose, sucrose, lactose, stachyose, and trehalose. Deletion of UvCCHC5 did not affect the expression of rice genes associated with grain filling, as revealed by RT-qPCR. We propose that the ∆UvCCHC5 mutants are impaired in transmembrane transport, and the resulting nutrient deficiencies prevent them from using nutrients from rice to form smut balls. RNA-seq data analysis indicated that UvCCHC4 affects the expression of genes involved in mitochondrial biogenesis, ribosomes, transporters, and ribosome biogenesis. These findings improve our understanding of the molecular mechanism underlying smut ball formation in rice by U. virens.
Highlights
Transcription factors are essential players in the development and virulence of plant pathogens that directly or indirectly regulate the expression of downstream genes [1]
Fungi 2021, 7, x FOR PEER REVIEWor UvCCHC7 grew normally and appeared blue on standard deviation (SD)/–Trp/–His plates, revealing t6raonf 1s9activation activity in yeast (Figure 1C). These results suggest that UvCCHC3, UvCCHC4, UvCCHC5, and UvCCHC7 function as transcription factors in U. virens
The virulence of the ∆UvCCHC4 and ∆UvCCHC5 mutants was significantly reduced, as ∆UvCCHC4 produced only approximately 24 smut balls on rice spikelets (Figure 5), and the ∆UvCCHC5 mutants failed to produce smut balls. These results indicate that UvCCHC6 and UvCCHC7 negatively regulate the virulence of U. virens, UvCCHC4 and UvCCHC5 positively regulate the virulence of this pathogen, and UvCCHC1, UvCCHC2, and UvCCHC3 have no effect on its virulence
Summary
Transcription factors are essential players in the development and virulence of plant pathogens that directly or indirectly regulate the expression of downstream genes [1]. The transcription factor families involved in phytopathogen development and virulence include bZIP (basic leucine zipper), bHLH (basic helix-loop-helix), homeodomain-like, MYB, MADS-box, APSES, and zinc-finger proteins [2]. Zinc-finger proteins use finger-like structures containing Zn2+ to bind DNA or RNA nucleotides and recognize DNA–RNA complexes or other proteins [3], thereby regulating the transcription or translation of genes that function in crucial processes such as growth, apoptosis, cell proliferation, and differentiation. Zinc-finger proteins are divided into different types based on their number and arrangement of Cys and His residues, such as C2HC, C2H2, C3HC4, C2HC5, and so on [4], as well as CCHC-type zinc finger proteins
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