The potato cyst nematode effector RHA1B is a ubiquitin ligase and uses two distinct mechanisms to suppress plant immune signaling

Abstract

Plant pathogens, such as bacteria, fungi, oomycetes and nematodes, rely on wide range of virulent effectors delivered into host cells to suppress plant immunity. Although phytobacterial effectors have been intensively investigated, little is known about the function of effectors of plant-parasitic nematodes, such as Globodera pallida , a cyst nematode responsible for vast losses in the potato and tomato industries. Here, we demonstrate using in vivo and in vitro ubiquitination assays the potato cyst nematode ( Globodera pallida ) effector RHA1B is an E3 ubiquitin ligase that employs multiple host plant E2 ubiquitin conjugation enzymes to catalyze ubiquitination. RHA1B was able to suppress effector-triggered immunity (ETI), as manifested by suppression of hypersensitive response (HR) mediated by a broad range of nucleotide-binding leucine-rich repeat (NB-LRR) immune receptors, presumably via E3-dependent degradation of the NB-LRR receptors. RHA1B also blocked the flg22-triggered expression of Acre31 and WRKY22 , marker genes of pathogen‐associated molecular pattern (PAMP)‐triggered immunity (PTI), but this did not require the E3 activity of RHA1B. Moreover, transgenic potato overexpressing the RHA1B transgene exhibited enhanced susceptibility to G . pallida . Thus, our data suggest RHA1B facilitates nematode parasitism not only by triggering degradation of NB-LRR immune receptors to block ETI signaling but also by suppressing PTI signaling via an as yet unknown E3-independent mechanism.

Diversity, Function and Regulation of Cell Surface and Intracellular Immune Receptors in Solanaceae

“…This is consistent with studies in Arabidopsis showing direct interaction between NLRs and the PRR FLS2 [167]. Therefore, it comes as no surprise that these two immune receptor types could be directly targeted and suppressed by a common pathogen effector, as shown in potato plants [168].…”

“…Plants 2020, x FOR PEER REVIEW 11 of 24 could be directly targeted and suppressed by a common pathogen effector, as shown in potato plants [168]. The transcription factor CAMTA (calmodulin binding transcription activator) has been identified as a convergent master transcription factor by negatively regulating both PTI-and ETIassociated genes in Arabidopsis [169].…”

The mechanism of potato resistance to Globodera rostochiensis: comparison of root transcriptomes of resistant and susceptible Solanum phureja genotypes

“…The natural variety of resistance mechanisms against potato sedentary nematodes has not been evaluated yet. Recent studies highlighted the biological complexity of plant-nematode interactions, for example the role of unusual R genes (such as soybean Rhg1 alpha-SNAP proteins efficient against a wide variety of cyst nematodes) [20,21], new nematode effectors and related mechanisms of immunity suppression (e.g., RHA1B) [22].…”

The effector GpRbp‐1 of Globodera pallida targets a nuclear HECT E3 ubiquitin ligase to modulate gene expression in the host

“…CEP12, a carboxyl extension protein processed from GrUBCEP12, supresses immunity mediated by intracellular immune receptors (Chronis et al , ). In addition, effector RHAB1 from G. pallida was recently reported to function as a RING‐type E3 ligase in planta and to promote susceptibility to the nematode (Kud et al , ). The recruitment of different components of the ubiquitination machinery by nematodes might suggest that potato cyst nematodes employ a multilayered strategy to exploit the UPS system of the host.…”

“…Conversely, the ubiquitination machinery of plants can be hijacked or mimicked by pathogens to aid in the infection process, for instance by the Avr3a effector from Phytophtora infestans or by AvrPtoB from Pseudomonas syringae (Abramovitch et al , ; Banfield, ; Bos et al , ). Nevertheless, the role of ubiquitination during recognition and responses to nematode invasion remains largely unexplored (Chronis et al , ; Hewezi, ; Kud et al , ).…”