Nonhost Resistance of Tomato to the Bean Pathogen Pseudomonas syringae pv. syringae B728a Is Due to a Defective E3 Ubiquitin Ligase Domain in AvrPtoBB728a

The bean pathogen Pseudomonas syringae pv. syringae B728a expresses homologs of the type III effectors AvrPto and AvrPtoB, either of which can trigger resistance in tomato cultivars expressing Pto and Prf genes. We found that strain B728a also elicits nonhost resistance in tomato cultivars VFNT Cher...

Full description

Bibliographic Details
Main Authors: Ching-Fang Chien, Johannes Mathieu, Chun-Hua Hsu, Patrick Boyle, Gregory B. Martin, Nai-Chun Lin
Format: Article
Language:English
Published: The American Phytopathological Society 2013-04-01
Series:Molecular Plant-Microbe Interactions
Online Access:https://apsjournals.apsnet.org/doi/10.1094/MPMI-08-12-0190-R
_version_ 1818915217733582848
author Ching-Fang Chien
Johannes Mathieu
Chun-Hua Hsu
Patrick Boyle
Gregory B. Martin
Nai-Chun Lin
author_facet Ching-Fang Chien
Johannes Mathieu
Chun-Hua Hsu
Patrick Boyle
Gregory B. Martin
Nai-Chun Lin
author_sort Ching-Fang Chien
collection DOAJ
description The bean pathogen Pseudomonas syringae pv. syringae B728a expresses homologs of the type III effectors AvrPto and AvrPtoB, either of which can trigger resistance in tomato cultivars expressing Pto and Prf genes. We found that strain B728a also elicits nonhost resistance in tomato cultivars VFNT Cherry and Moneymaker that lack Pto but express other members of the Pto family (e.g., SlFen and SlPtoC). Here, we show that the AvrPtoB homolog from B728a, termed AvrPtoBB728a (also known as HopAB1), is recognized by ‘VFNT Cherry’ and ‘Moneymaker’ when the effector is expressed in P. syringae pv. syringae 61, a strain lacking the avrPto or avrPtoB homolog. Using a gene-silencing approach, this recognition was shown to involve one or more Pto family members and Prf. AvrPtoBB728a interacted with SlFen, SlPtoC, and SlPtoD, in addition to Pto, in a yeast two-hybrid assay. In P. syringae pv. tomato DC3000, the C-terminal domain of AvrPtoB is an E3 ubiquitin ligase that ubiquitinates Fen, causing its degradation and leading to disease susceptibility. Although the C-terminal domain of AvrPtoBB728a shares 69% amino acid identity with that of AvrPtoB, we found that it has greatly reduced E3 ligase activity and is unable to ubiquitinate Fen in an in vitro ubiquitination assay. Thus, the nonhost resistance of ‘VFNT Cherry’ and ‘Moneymaker’ to B728a appears to be due to recognition of AvrPtoBB728 as a result of the effector's reduced E3 ligase activity, which prevents it from facilitating degradation of a Pto family member. We speculate that the primary plant host of B728a lacks a Fen-like protein and that, therefore, the E3 ligase of AvrPtoBB728 was unnecessary for pathogenicity and has diverged and become ineffective.
first_indexed 2024-12-19T23:58:46Z
format Article
id doaj.art-3a1289fdb6784731a7ed8d4923355429
institution Directory Open Access Journal
issn 0894-0282
1943-7706
language English
last_indexed 2024-12-19T23:58:46Z
publishDate 2013-04-01
publisher The American Phytopathological Society
record_format Article
series Molecular Plant-Microbe Interactions
spelling doaj.art-3a1289fdb6784731a7ed8d49233554292022-12-21T20:00:54ZengThe American Phytopathological SocietyMolecular Plant-Microbe Interactions0894-02821943-77062013-04-0126438739710.1094/MPMI-08-12-0190-RNonhost Resistance of Tomato to the Bean Pathogen Pseudomonas syringae pv. syringae B728a Is Due to a Defective E3 Ubiquitin Ligase Domain in AvrPtoBB728aChing-Fang ChienJohannes MathieuChun-Hua HsuPatrick BoyleGregory B. MartinNai-Chun LinThe bean pathogen Pseudomonas syringae pv. syringae B728a expresses homologs of the type III effectors AvrPto and AvrPtoB, either of which can trigger resistance in tomato cultivars expressing Pto and Prf genes. We found that strain B728a also elicits nonhost resistance in tomato cultivars VFNT Cherry and Moneymaker that lack Pto but express other members of the Pto family (e.g., SlFen and SlPtoC). Here, we show that the AvrPtoB homolog from B728a, termed AvrPtoBB728a (also known as HopAB1), is recognized by ‘VFNT Cherry’ and ‘Moneymaker’ when the effector is expressed in P. syringae pv. syringae 61, a strain lacking the avrPto or avrPtoB homolog. Using a gene-silencing approach, this recognition was shown to involve one or more Pto family members and Prf. AvrPtoBB728a interacted with SlFen, SlPtoC, and SlPtoD, in addition to Pto, in a yeast two-hybrid assay. In P. syringae pv. tomato DC3000, the C-terminal domain of AvrPtoB is an E3 ubiquitin ligase that ubiquitinates Fen, causing its degradation and leading to disease susceptibility. Although the C-terminal domain of AvrPtoBB728a shares 69% amino acid identity with that of AvrPtoB, we found that it has greatly reduced E3 ligase activity and is unable to ubiquitinate Fen in an in vitro ubiquitination assay. Thus, the nonhost resistance of ‘VFNT Cherry’ and ‘Moneymaker’ to B728a appears to be due to recognition of AvrPtoBB728 as a result of the effector's reduced E3 ligase activity, which prevents it from facilitating degradation of a Pto family member. We speculate that the primary plant host of B728a lacks a Fen-like protein and that, therefore, the E3 ligase of AvrPtoBB728 was unnecessary for pathogenicity and has diverged and become ineffective.https://apsjournals.apsnet.org/doi/10.1094/MPMI-08-12-0190-R
spellingShingle Ching-Fang Chien
Johannes Mathieu
Chun-Hua Hsu
Patrick Boyle
Gregory B. Martin
Nai-Chun Lin
Nonhost Resistance of Tomato to the Bean Pathogen Pseudomonas syringae pv. syringae B728a Is Due to a Defective E3 Ubiquitin Ligase Domain in AvrPtoBB728a
Molecular Plant-Microbe Interactions
title Nonhost Resistance of Tomato to the Bean Pathogen Pseudomonas syringae pv. syringae B728a Is Due to a Defective E3 Ubiquitin Ligase Domain in AvrPtoBB728a
title_full Nonhost Resistance of Tomato to the Bean Pathogen Pseudomonas syringae pv. syringae B728a Is Due to a Defective E3 Ubiquitin Ligase Domain in AvrPtoBB728a
title_fullStr Nonhost Resistance of Tomato to the Bean Pathogen Pseudomonas syringae pv. syringae B728a Is Due to a Defective E3 Ubiquitin Ligase Domain in AvrPtoBB728a
title_full_unstemmed Nonhost Resistance of Tomato to the Bean Pathogen Pseudomonas syringae pv. syringae B728a Is Due to a Defective E3 Ubiquitin Ligase Domain in AvrPtoBB728a
title_short Nonhost Resistance of Tomato to the Bean Pathogen Pseudomonas syringae pv. syringae B728a Is Due to a Defective E3 Ubiquitin Ligase Domain in AvrPtoBB728a
title_sort nonhost resistance of tomato to the bean pathogen pseudomonas syringae pv syringae b728a is due to a defective e3 ubiquitin ligase domain in avrptobb728a
url https://apsjournals.apsnet.org/doi/10.1094/MPMI-08-12-0190-R
work_keys_str_mv AT chingfangchien nonhostresistanceoftomatotothebeanpathogenpseudomonassyringaepvsyringaeb728aisduetoadefectivee3ubiquitinligasedomaininavrptobb728a
AT johannesmathieu nonhostresistanceoftomatotothebeanpathogenpseudomonassyringaepvsyringaeb728aisduetoadefectivee3ubiquitinligasedomaininavrptobb728a
AT chunhuahsu nonhostresistanceoftomatotothebeanpathogenpseudomonassyringaepvsyringaeb728aisduetoadefectivee3ubiquitinligasedomaininavrptobb728a
AT patrickboyle nonhostresistanceoftomatotothebeanpathogenpseudomonassyringaepvsyringaeb728aisduetoadefectivee3ubiquitinligasedomaininavrptobb728a
AT gregorybmartin nonhostresistanceoftomatotothebeanpathogenpseudomonassyringaepvsyringaeb728aisduetoadefectivee3ubiquitinligasedomaininavrptobb728a
AT naichunlin nonhostresistanceoftomatotothebeanpathogenpseudomonassyringaepvsyringaeb728aisduetoadefectivee3ubiquitinligasedomaininavrptobb728a