Research Article: The E3 Ligase APIP10 Connects the Effector AvrPiz-t to the NLR Receptor Piz-t in Rice

Date Published: March 31, 2016

Publisher: Public Library of Science

Author(s): Chan Ho Park, Gautam Shirsekar, Maria Bellizzi, Songbiao Chen, Pattavipha Songkumarn, Xin Xie, Xuetao Shi, Yuese Ning, Bo Zhou, Pavinee Suttiviriya, Mo Wang, Kenji Umemura, Guo-Liang Wang, Savithramma P. Dinesh-Kumar.


Although nucleotide-binding domain, leucine-rich repeat (NLR) proteins are the major immune receptors in plants, the mechanism that controls their activation and immune signaling remains elusive. Here, we report that the avirulence effector AvrPiz-t from Magnaporthe oryzae targets the rice E3 ligase APIP10 for degradation, but that APIP10, in return, ubiquitinates AvrPiz-t and thereby causes its degradation. Silencing of APIP10 in the non-Piz-t background compromises the basal defense against M. oryzae. Conversely, silencing of APIP10 in the Piz-t background causes cell death, significant accumulation of Piz-t, and enhanced resistance to M. oryzae, suggesting that APIP10 is a negative regulator of Piz-t. We show that APIP10 promotes degradation of Piz-t via the 26S proteasome system. Furthermore, we demonstrate that AvrPiz-t stabilizes Piz-t during M. oryzae infection. Together, our results show that APIP10 is a novel E3 ligase that functionally connects the fungal effector AvrPiz-t to its NLR receptor Piz-t in rice.

Partial Text

Unlike animal responses to pathogen infection, plant responses to pathogen infection do not include a circulatory system or specialized cells [1]. Instead, individual plant cells launch defense responses against invading pathogens. Extensive molecular studies over the last two decades have revealed two layers of host immunity in plants. Plant immunity can be activated when highly conserved pathogen-associated molecular patterns (PAMPs) are recognized by plasma membrane-bound pattern recognition receptors (PRRs) in a process called PAMP-triggered immunity (PTI). PTI is considered the first layer of plant immunity [2,3]. For the second layer, immunity can be activated when pathogen-delivered avirulence (Avr) effectors are recognized by the product of plant resistance (R) genes in a process called effector-triggered immunity (ETI). ETI can be achieved by the direct or indirect interaction between the Avr effectors and R proteins in the plant cell [1,4]. Upon recognition, both immunity layers are capable of initiating a signaling cascade that can result in multiple defense responses.

In host–microbe interactions, ubiquitination plays an important role in both host defense and pathogen infection [18,36]. Researchers have identified both pathogen effectors that target the ubiquitination machinery for defense suppression and plant ubiquitination-related proteins that target pathogen effectors for degradation and thus for defense enhancement. Most of these findings, however, have been derived from several model plant diseases caused by bacterial pathogens. Although recent research has revealed the importance of ubiquitination in plant diseases caused by fungi or oomycetes [20,37], the role of ubiquitination in these diseases is poorly understood. In particular, how microbial perturbation of host ubiquitination activates the defense response mediated by NLR receptor proteins is largely unknown. In this study, we describe the relationship among the fungal effector AvrPiz-t, the rice RING finger E3 ligase APIP10, and the NLR receptor Piz-t. We found that AvrPiz-t can interact with and promote the degradation of APIP10 when it is secreted into rice cells by M. oryzae. Silencing of APIP10 in the Piz-t background causes severe cell death and accumulation of Piz-t. Co-infiltration assays showed that APIP10 expression leads to Piz-t degradation and that such degradation depends on the RING finger domain of APIP10. In contrast, AvrPiz-t can stabilize Piz-t during blast infection. These results demonstrate an elegant defense mechanism in which rice cells use the E3 ligase APIP10 to regulate Piz-t for immune responses when attacked by the blast fungus carrying the AvrPiz-t gene. Degradation of the APIP10 by AvrPiz-t and the resulting elimination of the negative regulation of Piz-t protein by APIP10 leads to a rapid increase in Piz-t and a strong defense response including programmed cell death in the infected cells. Although APIP10 seems similar to RIN4 in Arabidopsis in that they both negatively regulate an NLR [7], the ability of APIP10 to degrade a pathogen effector (AvrPiz-t) and to regulate a host NLR (Piz-t) is unique. Therefore, identification of the novel E3 ligase APIP10 that functionally connects a fungal effector to its cognate NLR receptor in rice provides new insights into plant innate immunity.




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