TAL effectors: function, structure, engineering and applications

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TAL effectors are proteins secreted by bacterial pathogens into plant cells, where they enter the nucleus and activate expression of individual genes. TAL effectors display a modular architecture that includes a central DNA-binding region comprising a tandem array of nearly identical repeats that are almost all 34 residues long. Residue number 13 in each TAL repeat (one of two consecutive polymorphic amino acids that are termed ‘repeat variable diresidues’, or ‘RVDs’) specifies the identity of a single base; collectively the sequential repeats and their RVDs dictate the recognition of sequential bases along one of the two DNA strands. The modular architecture of TAL effectors has facilitated their extremely rapid development and application as artificial gene targeting reagents, particularly in the form of site-specific nucleases. Recent crystallographic and biochemical analyses of TAL effectors have established the structural basis of their DNA recognition properties and provide clear directions for future research.

Highlights

► TAL effectors are highly modular, easily programmable gene targeting proteins. ► Recent crystallographic analyses of TAL effectors have illustrated the basis for DNA recognition. ► Site-specific gene modification reagents using TAL effector scaffolds have recently been reported. ► The mechanism of target site search and acquisition by TAL effectors is an important question.

Section snippets

Historical background

TAL effectors are trans-kingdom transcription factors that are secreted by plant pathogenic bacteria in the genus Xanthomonas [1, 2]. Diseases caused by the many species and pathovars of Xanthomonas collectively affect a wide variety of plants, including several major crop and ornamental species [3], and their TAL effectors play critical roles in determining whether the bacterium is able to infect its host. The first TAL effector identified was AvrBs3 from Xanthomonas campestris pv. vesicatoria

Recognition code and initial structural analyses

The number of repeats found in TAL effectors varies from five to over thirty, with an average of roughly 17 [1]. Almost all are 34 amino acids in length, and they vary primarily in the identity of the residues at position 12 and 13 in each repeat, a pair of residues that were termed the ‘repeat variable diresidue’ or ‘RVD’. The repeat region always terminates with an apparently truncated repeat, containing the first 20 residues (including the RVD), which is commonly referred to as a ‘half

Recognition mechanism

Both crystal structures also demonstrated that sequence-specific contacts between the effector and the DNA are formed solely by the second residue of each RVD (at position 13 in each repeat) to atoms on the major groove edge of each base on a single contiguous strand of the DNA target. In contrast, the first residue in each RVD (position 12, which is usually occupied by an asparagine or a histidine) serves a largely structural role, forming a hydrogen bond between the side chain and the

Engineering and applications

The biological, bioinformatic and structural studies summarized above have led to an explosion of reports, starting with the initial description of a chimeric TAL effector nuclease in 2010 [37••], that demonstrate the successful creation of a wide variety of gene-targeting reagents using the TAL effector scaffold, as well as a variety of efficient methods for the rapid creation of such reagents that contain investigator-designed, artificial TAL repeat sequences (recently reviewed in [38, 39, 40

References and recommended reading

Papers of particular interest, published within the period of review, have been highlighted as:

  • • of special interest

  • •• of outstanding interest

Acknowledgements

The authors’ work in this field has been supported by the NIH (R01 GM098861 to A.J.B. and B.L.S. and R01 GM088277 to P.H.B.), a Searles Scholars Fellowship to P.H.B. and by training grant support from the Northwest Genome Engineering Consortium to A.N-S.M.

References (52)

  • A.J. Bogdanove et al.

    TAL effectors: finding plant genes for disease and defense

    Curr Opin Plant Biol

    (2010)
  • G. Van den Ackerveken et al.

    Recognition of the bacterial avirulence protein AvrBs3 occurs inside the host plant cell

    Cell

    (1996)
  • C. Tong et al.

    Rapid and cost-effective gene targeting in rat embryonic stem cells by TALENs

    J Genet Genomics

    (2012)
  • J. Boch et al.

    Xanthomonas AvrBs3 family-type III effectors: discovery and function

    Annu Rev Phytopathol

    (2010)
  • J. Mansfield et al.

    Top 10 plant pathogenic bacteria in molecular plant pathology

    Mol Plant Pathol

    (2012)
  • U. Bonas et al.

    Genetic and structural characterization of the avirulence gene avrBs3 from Xanthomonas campestris pv. vesicatoria

    Mol Gen Genet

    (1989)
  • V. Knoop 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

    J Bacteriol

    (1991)
  • R.D. De Feyter et al.

    Gene-for-genes interactions between cotton R genes and Xanthomonas campestris pv. malvacearumavr genes

    Mol Plant Microbe Interact

    (1993)
  • C.M. Hopkins et al.

    Identification of a family of avirulence genes from Xanthomonas oryzae pv. oryzae

    Mol Plant Microbe Interact

    (1992)
  • S. Swarup et al.

    A pathogenicity locus from Xanthomonas citri enables strains from several pathovars of Xanthomonas campestris to elicit canker-like lesions on citrus

    Phytopathology

    (1991)
  • J. Bai et al.

    Xanthomonasoryzae pv. oryzae avirulence genes contribute differently and specifically to pathogen aggressiveness

    Mol Plant Microbe Interact

    (2000)
  • S. Swarup et al.

    A Xanthomonas citri pathogenicity gene pthA pleiotropically encodes gratuitous avirulence on nonhosts

    Mol Plant Microbe Interact

    (1992)
  • H. Heuer et al.

    Repeat domain diversity of avrBs3-like genes in Ralstonia solanacearum strains and association with host preferences in the field

    Appl Environ Microbiol

    (2007)
  • Y. Yang et al.

    Xanthomonas avirulence-pathogenicity gene family encodes functional plant nuclear targeting signals

    Mol Plant Microbe Interact

    (1995)
  • B. Yang 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

    Proc Natl Acad Sci U S A

    (2000)
  • W. Zhu et al.

    AvrXa10 contains an acidic transcriptional activation domain in the functionally conserved C terminus

    Mol Plant Microbe Interact

    (1998)
  • W. Zhu et al.

    The C terminus of AvrXa10 can be replaced by the transcriptional activation domain of VP16 from the herpes simplex virus

    Plant Cell

    (1999)
  • A. Sugio et al.

    Two type III effector genes of Xanthomonas oryzae pv. oryzae control the induction of the host genes OsTFIIAgamma1 and OsTFX1 during bacterial blight of rice

    Proc Natl Acad Sci U S A

    (2007)
  • A.S. Iyer et al.

    The rice bacterial blight resistance gene xa5 encodes a novel form of disease resistance

    Mol Plant Microbe Interact

    (2004)
  • K. Gu et al.

    R gene expression induced by a type-III effector triggers disease resistance in rice

    Nature

    (2005)
  • B. Yang et al.

    Os8N3 is a host disease-susceptibility gene for bacterial blight of rice

    Proc Natl Acad Sci U S A

    (2006)
  • Z. Chu et al.

    Promoter mutations of an essential gene for pollen development result in disease resistance in rice

    Genes Dev

    (2006)
  • B. Yang et al.

    Avoidance of host recognition by alterations in the repetitive and C-terminal regions of AvrXa7, a type III effector of Xanthomonas oryzae pv. oryzae

    Mol Plant Microbe Interact

    (2005)
  • P. Romer et al.

    Plant pathogen recognition mediated by promoter activation of the pepper Bs3 resistance gene

    Science

    (2007)
  • S. Kay et al.

    A bacterial effector acts as a plant transcription factor and induces a cell size regulator

    Science

    (2007)
  • J. Boch et al.

    Breaking the code of DNA binding specificity of TAL-type III effectors

    Science

    (2009)

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