Citrus MAF1, a Repressor of RNA Polymerase III, Binds the Xanthomonas citri Canker Elicitor PthA4 and Suppresses Citrus Canker Development

• Published in: Plant physiology (Bethesda) Vol. 163; no. 1; pp. 232 - 242
• Main Authors: Soprano, Adriana Santos, Abe, Valeria Yukari, Smetana, Juliana Helena Costa, Benedetti, Celso Eduardo
• Format: Journal Article
• Language: English
• Published: Rockville, MD American Society of Plant Biologists 01.09.2013
• Subjects: Amino Acid Sequence; Bacterial plant pathogens; Biological and medical sciences; Cell growth; Citrus - genetics; Citrus - microbiology; Citrus - physiology; Conserved Sequence; Fundamental and applied biological sciences. Psychology; Genes; GENES, DEVELOPMENT, AND EVOLUTION; Humans; Leaves; Lesions; Molecular Sequence Data; Phylogeny; Phytopathology. Animal pests. Plant and forest protection; Plant Diseases - genetics; Plant physiology and development; Plant Proteins - genetics; Plant Proteins - metabolism; Plant Proteins - physiology; Plants; Proteins; Repressor Proteins - chemistry; RNA; RNA Polymerase III - antagonists & inhibitors; Saccharomyces cerevisiae - genetics; Sequence Alignment; Transfer RNA; Xanthomonas; Yeasts; Pseudomonadales; Plant pathogen; Enzyme; Transferases; Citrus fruit; Rutaceae; Repression; Elicitor; DNA-directed RNA polymerase; Infection; Citrus; Nucleotidyltransferases; Plant physiology; Dicotyledones; Angiospermae; Xanthomonas campestris pv. citri; Bacteriosis; Development; Bacteria; Pseudomonadaceae; Spermatophyta
• ISSN: 0032-0889; 1532-2548
• DOI: 10.1104/pp.113.224642

Transcription activator-like (TAL) effectors from Xanthomonas species pathogens act as transcription factors in plant cells; however, how TAL effectors activate host transcription is unknown. We found previously that TAL effectors of the citrus canker pathogen Xanthomonas citri, known as PthAs, bind the carboxyl-terminal domain of the sweet orange (Citrus sinensis) RNA polymerase II (Pol II) and inhibit the activity of CsCYP, a cyclophilin associated with the carboxyl-terminal domain of the citrus RNA Pol II that functions as a negative regulator of cell growth. Here, we show that PthA4 specifically interacted with the sweet orange MAF1 (CsMAF1) protein, an RNA polymerase III (Pol III) repressor that controls ribosome biogenesis and cell growth in yeast (Saccharomyces cerevisiae) and human. CsMAF1 bound the human RNA Pol III and rescued the yeast maf1 mutant by repressing tRNA His transcription. The expression of PthA4 in the maf1 mutant slightly restored tRNA His synthesis, indicating that PthA4 counteracts CsMAF1 activity. In addition, we show that sweet orange RNA interference plants with reduced CsMAF1 levels displayed a dramatic increase in tRNA transcription and a marked phenotype of cell proliferation during canker formation. Conversely, CsMAF1 overexpression was detrimental to seedling growth, inhibited tRNA synthesis, and attenuated canker development. Furthermore, we found that PthA4 is required to elicit cankers in sweet orange leaves and that depletion of CsMAF1 in X. citri-infected tissues correlates with the development of hyperplastic lesions and the presence of PthA4. Considering that CsMAF1 and CsCYP function as canker suppressors in sweet orange, our data indicate that TAL effectors from X. citri target negative regulators of RNA Pol II and Pol III to coordinately increase the transcription of host genes involved in ribosome biogenesis and cell proliferation.