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...
Main Authors: | , , , , , |
---|---|
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 |