Targeted promoter editing for rice resistance to Xanthomonas oryzae pv. oryzae reveals differential activities for SWEET14-inducing TAL effectors

Research output: Contribution to journalArticleResearchpeer review

Authors

  • Servane Blanvillain-Baufumé
  • Maik Reschke
  • Montserrat Solé
  • Florence Auguy
  • Hinda Doucoure
  • Boris Szurek
  • Donaldo Meynard
  • Murielle Portefaix
  • Sébastien Cunnac
  • Emmanuel Guiderdoni
  • Jens Boch
  • Ralf Koebnik

External Research Organisations

  • French Agricultural Research Centre for International Development (CIRAD)
  • Martin Luther University Halle-Wittenberg
  • UMR AGAP (Amélioration génétique et Adaptation des Plantes)
View graph of relations

Details

Original languageEnglish
Pages (from-to)306-317
Number of pages12
JournalPlant Biotechnology Journal
Volume15
Issue number3
Publication statusPublished - 19 Aug 2016
Externally publishedYes

Abstract

As a key virulence strategy to cause bacterial leaf blight, Xanthomonas oryzae pv. oryzae (Xoo) injects into the plant cell DNA-binding proteins called transcription activator-like effectors (TALEs) that bind to effector-binding elements (EBEs) in a sequence-specific manner, resulting in host gene induction. TALEs AvrXa7, PthXo3, TalC and Tal5, found in geographically distant Xoo strains, all target OsSWEET14, thus considered as a pivotal TALE target acting as major susceptibility factor during rice–Xoo interactions. Here, we report the generation of an allele library of the OsSWEET14 promoter through stable expression of TALE-nuclease (TALEN) constructs in rice. The susceptibility level of lines carrying mutations in AvrXa7, Tal5 or TalC EBEs was assessed. Plants edited in AvrXa7 or Tal5 EBEs were resistant to bacterial strains relying on the corresponding TALE. Surprisingly, although indels within TalC EBE prevented OsSWEET14 induction in response to BAI3 wild-type bacteria relying on TalC, loss of TalC responsiveness failed to confer resistance to this strain. The TalC EBE mutant line was, however, resistant to a strain expressing an artificial SWEET14-inducing TALE whose EBE was also edited in this line. This work offers the first set of alleles edited in TalC EBE and uncovers a distinct, broader range of activities for TalC compared to AvrXa7 or Tal5. We propose the existence of additional targets for TalC beyond SWEET14, suggesting that TALE-mediated plant susceptibility may result from induction of several, genetically redundant, host susceptibility genes by a single effector.

Keywords

    bacterial leaf blight, genome engineering, susceptibility gene, TALEN, transgene-free plants

ASJC Scopus subject areas

Cite this

Targeted promoter editing for rice resistance to Xanthomonas oryzae pv. oryzae reveals differential activities for SWEET14-inducing TAL effectors. / Blanvillain-Baufumé, Servane; Reschke, Maik; Solé, Montserrat et al.
In: Plant Biotechnology Journal, Vol. 15, No. 3, 19.08.2016, p. 306-317.

Research output: Contribution to journalArticleResearchpeer review

Blanvillain-Baufumé, S, Reschke, M, Solé, M, Auguy, F, Doucoure, H, Szurek, B, Meynard, D, Portefaix, M, Cunnac, S, Guiderdoni, E, Boch, J & Koebnik, R 2016, 'Targeted promoter editing for rice resistance to Xanthomonas oryzae pv. oryzae reveals differential activities for SWEET14-inducing TAL effectors', Plant Biotechnology Journal, vol. 15, no. 3, pp. 306-317. https://doi.org/10.1111/pbi.12613
Blanvillain-Baufumé, S., Reschke, M., Solé, M., Auguy, F., Doucoure, H., Szurek, B., Meynard, D., Portefaix, M., Cunnac, S., Guiderdoni, E., Boch, J., & Koebnik, R. (2016). Targeted promoter editing for rice resistance to Xanthomonas oryzae pv. oryzae reveals differential activities for SWEET14-inducing TAL effectors. Plant Biotechnology Journal, 15(3), 306-317. https://doi.org/10.1111/pbi.12613
Blanvillain-Baufumé S, Reschke M, Solé M, Auguy F, Doucoure H, Szurek B et al. Targeted promoter editing for rice resistance to Xanthomonas oryzae pv. oryzae reveals differential activities for SWEET14-inducing TAL effectors. Plant Biotechnology Journal. 2016 Aug 19;15(3):306-317. doi: 10.1111/pbi.12613
Blanvillain-Baufumé, Servane ; Reschke, Maik ; Solé, Montserrat et al. / Targeted promoter editing for rice resistance to Xanthomonas oryzae pv. oryzae reveals differential activities for SWEET14-inducing TAL effectors. In: Plant Biotechnology Journal. 2016 ; Vol. 15, No. 3. pp. 306-317.
Download
@article{018fc022b38549918da952b2c878964a,
title = "Targeted promoter editing for rice resistance to Xanthomonas oryzae pv. oryzae reveals differential activities for SWEET14-inducing TAL effectors",
abstract = "As a key virulence strategy to cause bacterial leaf blight, Xanthomonas oryzae pv. oryzae (Xoo) injects into the plant cell DNA-binding proteins called transcription activator-like effectors (TALEs) that bind to effector-binding elements (EBEs) in a sequence-specific manner, resulting in host gene induction. TALEs AvrXa7, PthXo3, TalC and Tal5, found in geographically distant Xoo strains, all target OsSWEET14, thus considered as a pivotal TALE target acting as major susceptibility factor during rice–Xoo interactions. Here, we report the generation of an allele library of the OsSWEET14 promoter through stable expression of TALE-nuclease (TALEN) constructs in rice. The susceptibility level of lines carrying mutations in AvrXa7, Tal5 or TalC EBEs was assessed. Plants edited in AvrXa7 or Tal5 EBEs were resistant to bacterial strains relying on the corresponding TALE. Surprisingly, although indels within TalC EBE prevented OsSWEET14 induction in response to BAI3 wild-type bacteria relying on TalC, loss of TalC responsiveness failed to confer resistance to this strain. The TalC EBE mutant line was, however, resistant to a strain expressing an artificial SWEET14-inducing TALE whose EBE was also edited in this line. This work offers the first set of alleles edited in TalC EBE and uncovers a distinct, broader range of activities for TalC compared to AvrXa7 or Tal5. We propose the existence of additional targets for TalC beyond SWEET14, suggesting that TALE-mediated plant susceptibility may result from induction of several, genetically redundant, host susceptibility genes by a single effector.",
keywords = "bacterial leaf blight, genome engineering, susceptibility gene, TALEN, transgene-free plants",
author = "Servane Blanvillain-Baufum{\'e} and Maik Reschke and Montserrat Sol{\'e} and Florence Auguy and Hinda Doucoure and Boris Szurek and Donaldo Meynard and Murielle Portefaix and S{\'e}bastien Cunnac and Emmanuel Guiderdoni and Jens Boch and Ralf Koebnik",
note = "Funding information: This work was funded by a Phase I {\textquoteleft}Grand Challenge Exploration Grant{\textquoteright} of the Bill and Melinda Gates Foundation (OPP1060078), an IRD postdoctoral fellowship attributed to SB-B, a {\textquoteleft}Chercheur d'Avenir{\textquoteright} grant from the Region Languedoc-Roussillon attributed to SC and a grant from the European Regional Development Fund of the European Commission to JB. This work benefited from interactions promoted by COST Action FA 1208 (https://www.cost-sustain.org).",
year = "2016",
month = aug,
day = "19",
doi = "10.1111/pbi.12613",
language = "English",
volume = "15",
pages = "306--317",
journal = "Plant Biotechnology Journal",
issn = "1467-7644",
publisher = "Wiley-Blackwell Publishing Ltd",
number = "3",

}

Download

TY - JOUR

T1 - Targeted promoter editing for rice resistance to Xanthomonas oryzae pv. oryzae reveals differential activities for SWEET14-inducing TAL effectors

AU - Blanvillain-Baufumé, Servane

AU - Reschke, Maik

AU - Solé, Montserrat

AU - Auguy, Florence

AU - Doucoure, Hinda

AU - Szurek, Boris

AU - Meynard, Donaldo

AU - Portefaix, Murielle

AU - Cunnac, Sébastien

AU - Guiderdoni, Emmanuel

AU - Boch, Jens

AU - Koebnik, Ralf

N1 - Funding information: This work was funded by a Phase I ‘Grand Challenge Exploration Grant’ of the Bill and Melinda Gates Foundation (OPP1060078), an IRD postdoctoral fellowship attributed to SB-B, a ‘Chercheur d'Avenir’ grant from the Region Languedoc-Roussillon attributed to SC and a grant from the European Regional Development Fund of the European Commission to JB. This work benefited from interactions promoted by COST Action FA 1208 (https://www.cost-sustain.org).

PY - 2016/8/19

Y1 - 2016/8/19

N2 - As a key virulence strategy to cause bacterial leaf blight, Xanthomonas oryzae pv. oryzae (Xoo) injects into the plant cell DNA-binding proteins called transcription activator-like effectors (TALEs) that bind to effector-binding elements (EBEs) in a sequence-specific manner, resulting in host gene induction. TALEs AvrXa7, PthXo3, TalC and Tal5, found in geographically distant Xoo strains, all target OsSWEET14, thus considered as a pivotal TALE target acting as major susceptibility factor during rice–Xoo interactions. Here, we report the generation of an allele library of the OsSWEET14 promoter through stable expression of TALE-nuclease (TALEN) constructs in rice. The susceptibility level of lines carrying mutations in AvrXa7, Tal5 or TalC EBEs was assessed. Plants edited in AvrXa7 or Tal5 EBEs were resistant to bacterial strains relying on the corresponding TALE. Surprisingly, although indels within TalC EBE prevented OsSWEET14 induction in response to BAI3 wild-type bacteria relying on TalC, loss of TalC responsiveness failed to confer resistance to this strain. The TalC EBE mutant line was, however, resistant to a strain expressing an artificial SWEET14-inducing TALE whose EBE was also edited in this line. This work offers the first set of alleles edited in TalC EBE and uncovers a distinct, broader range of activities for TalC compared to AvrXa7 or Tal5. We propose the existence of additional targets for TalC beyond SWEET14, suggesting that TALE-mediated plant susceptibility may result from induction of several, genetically redundant, host susceptibility genes by a single effector.

AB - As a key virulence strategy to cause bacterial leaf blight, Xanthomonas oryzae pv. oryzae (Xoo) injects into the plant cell DNA-binding proteins called transcription activator-like effectors (TALEs) that bind to effector-binding elements (EBEs) in a sequence-specific manner, resulting in host gene induction. TALEs AvrXa7, PthXo3, TalC and Tal5, found in geographically distant Xoo strains, all target OsSWEET14, thus considered as a pivotal TALE target acting as major susceptibility factor during rice–Xoo interactions. Here, we report the generation of an allele library of the OsSWEET14 promoter through stable expression of TALE-nuclease (TALEN) constructs in rice. The susceptibility level of lines carrying mutations in AvrXa7, Tal5 or TalC EBEs was assessed. Plants edited in AvrXa7 or Tal5 EBEs were resistant to bacterial strains relying on the corresponding TALE. Surprisingly, although indels within TalC EBE prevented OsSWEET14 induction in response to BAI3 wild-type bacteria relying on TalC, loss of TalC responsiveness failed to confer resistance to this strain. The TalC EBE mutant line was, however, resistant to a strain expressing an artificial SWEET14-inducing TALE whose EBE was also edited in this line. This work offers the first set of alleles edited in TalC EBE and uncovers a distinct, broader range of activities for TalC compared to AvrXa7 or Tal5. We propose the existence of additional targets for TalC beyond SWEET14, suggesting that TALE-mediated plant susceptibility may result from induction of several, genetically redundant, host susceptibility genes by a single effector.

KW - bacterial leaf blight

KW - genome engineering

KW - susceptibility gene

KW - TALEN

KW - transgene-free plants

UR - http://www.scopus.com/inward/record.url?scp=85013035920&partnerID=8YFLogxK

U2 - 10.1111/pbi.12613

DO - 10.1111/pbi.12613

M3 - Article

C2 - 27539813

AN - SCOPUS:85013035920

VL - 15

SP - 306

EP - 317

JO - Plant Biotechnology Journal

JF - Plant Biotechnology Journal

SN - 1467-7644

IS - 3

ER -