A Bacterial Effector Acts as a Plant Transcription Factor and Induces a Cell Size Regulator

Pathogenicity of many Gram-negative bacteria relies on the injection of effector proteins by type III secretion into eukaryotic cells, where they modulate host signaling pathways to the pathogen's benefit. One such effector protein injected by Xanthomonas into plants is AvrBs3, which localizes to the plant cell nucleus and causes hypertrophy of plant mesophyll cells. We show that AvrBs3 induces the expression of a master regulator of cell size, upa20, which encodes a transcription factor containing a basic helix-loop-helix domain. AvrBs3 binds to a conserved element in the upa20 promoter via its central repeat region and induces gene expression through its activation domain. Thus, AvrBs3 and likely other members of this family provoke developmental reprogramming of host cells by mimicking eukaryotic transcription factors.

[1]  E. Huq,et al.  The Arabidopsis Basic/Helix-Loop-Helix Transcription Factor Family Online version contains Web-only data. Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.013839. , 2003, The Plant Cell Online.

[2]  David L. Spector,et al.  Nuclear speckles: a model for nuclear organelles , 2003, Nature Reviews Molecular Cell Biology.

[3]  Simone Hahn,et al.  Plant Pathogen Recognition Mediated by Promoter Activation of the Pepper Bs3 Resistance Gene , 2007, Science.

[4]  U. Bonas,et al.  Dimerization of the bacterial effector protein AvrBs3 in the plant cell cytoplasm prior to nuclear import. , 2005, The Plant journal : for cell and molecular biology.

[5]  A Suyama,et al.  Diverse transcriptional initiation revealed by fine, large‐scale mapping of mRNA start sites , 2001, EMBO reports.

[6]  U. Bonas,et al.  Genetic and structural characterization of the avirulence gene avrBs3 from Xanthomonas campestris pv. vesicatoria , 1989, Molecular and General Genetics MGG.

[7]  F. White,et al.  Diverse members of the AvrBs3/PthA family of type III effectors are major virulence determinants in bacterial blight disease of rice. , 2004, Molecular plant-microbe interactions : MPMI.

[8]  J. Swings,et al.  The host range of the genusXanthomonas , 1984, The Botanical Review.

[9]  W. Zhu,et al.  The virulence factor AvrXa7 of Xanthomonas oryzae pv. oryzae is a type III secretion pathway-dependent nuclear-localized double-stranded DNA-binding protein. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[10]  M. Kokkinidis,et al.  Conserved features of type III secretion , 2004, Cellular microbiology.

[11]  C. Dumas,et al.  BIGPETALp, a bHLH transcription factor is involved in the control of Arabidopsis petal size , 2006, The EMBO journal.

[12]  Frank Thieme,et al.  Type III effector proteins from the plant pathogen Xanthomonas and their role in the interaction with the host plant. , 2006, Journal of plant physiology.

[13]  U. Bonas,et al.  Race-specificity of plant resistance to bacterial spot disease determined by repetitive motifs in a bacterial avirulence protein , 1992, Nature.

[14]  G. Van den Ackerveken,et al.  Eukaryotic features of the Xanthomonas type III effector AvrBs3: protein domains involved in transcriptional activation and the interaction with nuclear import receptors from pepper. , 2001, The Plant journal : for cell and molecular biology.

[15]  C. Glover,et al.  Gene expression profiling for hematopoietic cell culture , 2006 .

[16]  D. Gabriel,et al.  Watersoaking function(s) of XcmH1005 are redundantly encoded by members of the Xanthomonas avr/pth gene family , 1996 .

[17]  J. Bergelson,et al.  Effector genes of Xanthomonas axonopodis pv. vesicatoria promote transmission and enhance other fitness traits in the field. , 2004, Genetics.

[18]  R. Rosenfeld Nature , 2009, Otolaryngology--head and neck surgery : official journal of American Academy of Otolaryngology-Head and Neck Surgery.

[19]  H. Leung,et al.  Xanthomonas oryzae pv. oryzae avirulence genes contribute differently and specifically to pathogen aggressiveness. , 2000, Molecular plant-microbe interactions : MPMI.

[20]  U. Bonas,et al.  Type III‐dependent translocation of the Xanthomonas AvrBs3 protein into the plant cell , 2002, Molecular microbiology.

[21]  Fan Yang,et al.  R gene expression induced by a type-III effector triggers disease resistance in rice , 2005, Nature.

[22]  U. Bonas,et al.  The Xanthomonas Hrp type III system secretes proteins from plant and mammalian bacterial pathogens. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[23]  U. Bonas,et al.  Resistance in tomato to Xanthomonas campestris pv vesicatoria is determined by alleles of the pepper-specific avirulence gene avrBs3 , 1993, Molecular and General Genetics MGG.

[24]  R. Aloni,et al.  Comparative anatomy of gall development on Gypsophila paniculata induced by bacteria with different mechanisms of pathogenicity , 2006, Planta.

[25]  U. Bonas,et al.  Expression of the avirulence gene avrBs3 from Xanthomonas campestris pv. vesicatoria is not under the control of hrp genes and is independent of plant factors , 1991, Journal of bacteriology.

[26]  U. Bonas,et al.  Physical delimitation of the pepper Bs3 resistance gene specifying recognition of the AvrBs3 protein from Xanthomonas campestris pv. vesicatoria , 2006, Theoretical and Applied Genetics.

[27]  F. White,et al.  Os8N3 is a host disease-susceptibility gene for bacterial blight of rice , 2006, Proceedings of the National Academy of Sciences.

[28]  G. Erdos,et al.  Expression of a single, host-specific, bacterial pathogenicity gene in plant cells elicits division, enlargement, and cell death , 1999 .

[29]  Masaru Tomita,et al.  Computational analysis suggests that alternative first exons are involved in tissue-specific transcription in rice (Oryza sativa) , 2005, Bioinform..

[30]  宁北芳,et al.  疟原虫var基因转换速率变化导致抗原变异[英]/Paul H, Robert P, Christodoulou Z, et al//Proc Natl Acad Sci U S A , 2005 .

[31]  G. Van den Ackerveken,et al.  The xanthomonas type III effector protein AvrBs3 modulates plant gene expression and induces cell hypertrophy in the susceptible host. , 2002, Molecular plant-microbe interactions : MPMI.

[32]  U. Bonas,et al.  Recognition of the Bacterial Avirulence Protein AvrBs3 Occurs inside the Host Plant Cell , 1996, Cell.